diff --git a/codex-rs/Cargo.lock b/codex-rs/Cargo.lock
index dc109aeaba..d0767f4141 100644
--- a/codex-rs/Cargo.lock
+++ b/codex-rs/Cargo.lock
@@ -3309,6 +3309,7 @@ dependencies = [
  "landlock",
  "libc",
  "pretty_assertions",
+ "rustix 1.1.4",
  "seccompiler",
  "serde",
  "serde_json",
diff --git a/codex-rs/Cargo.toml b/codex-rs/Cargo.toml
index bc4330731d..8dadc1f0e4 100644
--- a/codex-rs/Cargo.toml
+++ b/codex-rs/Cargo.toml
@@ -388,6 +388,7 @@ rustls = { version = "0.23", default-features = false, features = [
 ] }
 rustls-native-certs = "0.8.3"
 rustls-pki-types = "1.14.0"
+rustix = { version = "1.1.4", features = ["thread"] }
 schemars = "0.8.22"
 seccompiler = "0.5.0"
 semver = "1.0"
diff --git a/codex-rs/linux-sandbox/Cargo.toml b/codex-rs/linux-sandbox/Cargo.toml
index 0f7c68a152..713e5d2cee 100644
--- a/codex-rs/linux-sandbox/Cargo.toml
+++ b/codex-rs/linux-sandbox/Cargo.toml
@@ -31,6 +31,7 @@ seccompiler = { workspace = true }
 serde = { workspace = true, features = ["derive"] }
 serde_json = { workspace = true }
 sha2 = { workspace = true }
+rustix = { workspace = true }
 url = { workspace = true }
 
 [target.'cfg(target_os = "linux")'.dev-dependencies]
diff --git a/codex-rs/linux-sandbox/src/dns_routing.rs b/codex-rs/linux-sandbox/src/dns_routing.rs
new file mode 100644
index 0000000000..0a0da59ab6
--- /dev/null
+++ b/codex-rs/linux-sandbox/src/dns_routing.rs
@@ -0,0 +1,173 @@
+use codex_network_proxy::DNS_PROXY_ENV_KEY;
+use codex_network_proxy::DNS_PROXY_SESSION_PREFACE;
+use std::io;
+use std::io::Read;
+use std::io::Write;
+use std::net::Ipv4Addr;
+use std::net::SocketAddr;
+use std::net::TcpListener;
+use std::net::TcpStream;
+use std::net::UdpSocket;
+use std::time::Duration;
+use url::Url;
+
+const SANDBOX_DNS_LISTEN_ADDR: (Ipv4Addr, u16) = (Ipv4Addr::LOCALHOST, 53);
+const DNS_IO_TIMEOUT: Duration = Duration::from_secs(3);
+const MAX_DNS_MESSAGE_BYTES: usize = usize::from(u16::MAX);
+
+pub(crate) struct BoundDnsStub {
+    udp_socket: UdpSocket,
+    tcp_listener: TcpListener,
+}
+
+pub(crate) fn bind_netns_dns_stub() -> io::Result<BoundDnsStub> {
+    let udp_socket = UdpSocket::bind(SANDBOX_DNS_LISTEN_ADDR)?;
+    let tcp_listener = TcpListener::bind(SANDBOX_DNS_LISTEN_ADDR)?;
+    Ok(BoundDnsStub {
+        udp_socket,
+        tcp_listener,
+    })
+}
+
+pub(crate) fn spawn_netns_dns_stub(bound: BoundDnsStub) -> io::Result<()> {
+    let endpoint = take_dns_proxy_endpoint_from_env()?.ok_or_else(|| {
+        io::Error::new(
+            io::ErrorKind::NotFound,
+            "DNS bridge expected a proxy endpoint",
+        )
+    })?;
+    let pid = unsafe { libc::fork() };
+    if pid < 0 {
+        return Err(io::Error::last_os_error());
+    }
+    if pid == 0 {
+        let status = i32::from(
+            crate::proxy_routing::harden_bridge_process()
+                .and_then(|_| run_netns_dns_stub(bound, endpoint))
+                .is_err(),
+        );
+        unsafe { libc::_exit(status) };
+    }
+    Ok(())
+}
+
+fn take_dns_proxy_endpoint_from_env() -> io::Result<Option<SocketAddr>> {
+    let Some(value) = std::env::var_os(DNS_PROXY_ENV_KEY) else {
+        return Ok(None);
+    };
+    // SAFETY: the helper process is single-threaded at this point, before execing
+    // the user command.
+    unsafe { std::env::remove_var(DNS_PROXY_ENV_KEY) };
+    let value = value
+        .into_string()
+        .map_err(|_| io::Error::new(io::ErrorKind::InvalidInput, "DNS proxy URL is not UTF-8"))?;
+    parse_dns_proxy_endpoint(value.as_str()).map(Some)
+}
+
+fn parse_dns_proxy_endpoint(value: &str) -> io::Result<SocketAddr> {
+    let parsed = Url::parse(value).map_err(|err| {
+        io::Error::new(
+            io::ErrorKind::InvalidInput,
+            format!("invalid DNS proxy URL: {err}"),
+        )
+    })?;
+    if parsed.scheme() != "tcp" {
+        return Err(io::Error::new(
+            io::ErrorKind::InvalidInput,
+            "DNS proxy URL must use tcp scheme",
+        ));
+    }
+    let Some(host) = parsed.host_str() else {
+        return Err(io::Error::new(
+            io::ErrorKind::InvalidInput,
+            "DNS proxy URL is missing host",
+        ));
+    };
+    if host != "127.0.0.1" {
+        return Err(io::Error::new(
+            io::ErrorKind::InvalidInput,
+            "DNS proxy URL must point at 127.0.0.1",
+        ));
+    }
+    let Some(port) = parsed.port() else {
+        return Err(io::Error::new(
+            io::ErrorKind::InvalidInput,
+            "DNS proxy URL is missing port",
+        ));
+    };
+    Ok(SocketAddr::from((Ipv4Addr::LOCALHOST, port)))
+}
+
+fn run_netns_dns_stub(bound: BoundDnsStub, endpoint: SocketAddr) -> io::Result<()> {
+    let udp_endpoint = endpoint;
+    std::thread::Builder::new().spawn(move || netns_udp_loop(bound.udp_socket, udp_endpoint))?;
+    netns_tcp_loop(bound.tcp_listener, endpoint)
+}
+
+fn netns_udp_loop(socket: UdpSocket, endpoint: SocketAddr) -> io::Result<()> {
+    let mut query = vec![0; MAX_DNS_MESSAGE_BYTES];
+    loop {
+        let (len, peer) = socket.recv_from(&mut query)?;
+        let response = resolve_through_proxy(endpoint, &query[..len])?;
+        socket.send_to(&response, peer)?;
+    }
+}
+
+fn netns_tcp_loop(listener: TcpListener, endpoint: SocketAddr) -> io::Result<()> {
+    loop {
+        let (mut client, _) = listener.accept()?;
+        client.set_read_timeout(Some(DNS_IO_TIMEOUT))?;
+        client.set_write_timeout(Some(DNS_IO_TIMEOUT))?;
+        std::thread::spawn(move || {
+            let _ = serve_tcp_client(&mut client, endpoint);
+        });
+    }
+}
+
+fn serve_tcp_client(client: &mut TcpStream, endpoint: SocketAddr) -> io::Result<()> {
+    while let Ok(query) = read_frame(client) {
+        let response = resolve_through_proxy(endpoint, &query)?;
+        write_frame(client, &response)?;
+    }
+    Ok(())
+}
+
+fn resolve_through_proxy(endpoint: SocketAddr, query: &[u8]) -> io::Result<Vec<u8>> {
+    let mut stream = TcpStream::connect(endpoint)?;
+    stream.set_read_timeout(Some(DNS_IO_TIMEOUT))?;
+    stream.set_write_timeout(Some(DNS_IO_TIMEOUT))?;
+    stream.write_all(DNS_PROXY_SESSION_PREFACE)?;
+    let mut ack = [0_u8; DNS_PROXY_SESSION_PREFACE.len()];
+    stream.read_exact(&mut ack)?;
+    if &ack != DNS_PROXY_SESSION_PREFACE {
+        return Err(io::Error::new(
+            io::ErrorKind::InvalidData,
+            "DNS proxy rejected session preface",
+        ));
+    }
+    write_frame(&mut stream, query)?;
+    read_frame(&mut stream)
+}
+
+fn write_frame(writer: &mut impl Write, payload: &[u8]) -> io::Result<()> {
+    let len = u16::try_from(payload.len()).map_err(|_| {
+        io::Error::new(
+            io::ErrorKind::InvalidInput,
+            "DNS message exceeds maximum wire length",
+        )
+    })?;
+    writer.write_all(&len.to_be_bytes())?;
+    writer.write_all(payload)
+}
+
+fn read_frame(reader: &mut impl Read) -> io::Result<Vec<u8>> {
+    let mut len = [0; 2];
+    reader.read_exact(&mut len)?;
+    let mut payload = vec![0; usize::from(u16::from_be_bytes(len))];
+    reader.read_exact(&mut payload)?;
+    Ok(payload)
+}
+
+#[cfg(test)]
+#[path = "dns_routing_tests.rs"]
+mod tests;
diff --git a/codex-rs/linux-sandbox/src/dns_routing_tests.rs b/codex-rs/linux-sandbox/src/dns_routing_tests.rs
new file mode 100644
index 0000000000..3a68f7bc9a
--- /dev/null
+++ b/codex-rs/linux-sandbox/src/dns_routing_tests.rs
@@ -0,0 +1,45 @@
+use super::*;
+use pretty_assertions::assert_eq;
+use std::net::TcpListener;
+use std::sync::mpsc;
+
+#[test]
+fn parses_loopback_dns_proxy_endpoint() {
+    assert_eq!(
+        parse_dns_proxy_endpoint("tcp://127.0.0.1:43128").expect("endpoint"),
+        SocketAddr::from((Ipv4Addr::LOCALHOST, 43128))
+    );
+}
+
+#[test]
+fn rejects_non_loopback_dns_proxy_endpoint() {
+    let err =
+        parse_dns_proxy_endpoint("tcp://192.0.2.10:43128").expect_err("non-loopback endpoint");
+    assert_eq!(err.kind(), io::ErrorKind::InvalidInput);
+}
+
+#[test]
+fn forwards_dns_query_to_private_proxy_session() {
+    let listener = TcpListener::bind((Ipv4Addr::LOCALHOST, 0)).expect("bind DNS proxy fixture");
+    let endpoint = listener.local_addr().expect("fixture local addr");
+    let (received_tx, received_rx) = mpsc::channel();
+    let expected_response = b"dns-response".to_vec();
+    let response = expected_response.clone();
+    std::thread::spawn(move || {
+        let (mut stream, _) = listener.accept().expect("accept DNS proxy session");
+        let mut preface = [0_u8; DNS_PROXY_SESSION_PREFACE.len()];
+        stream.read_exact(&mut preface).expect("read preface");
+        assert_eq!(&preface, DNS_PROXY_SESSION_PREFACE);
+        stream
+            .write_all(DNS_PROXY_SESSION_PREFACE)
+            .expect("write preface ack");
+        let query = read_frame(&mut stream).expect("read query");
+        received_tx.send(query).expect("send query");
+        write_frame(&mut stream, &response).expect("write response");
+    });
+
+    let response = resolve_through_proxy(endpoint, b"dns-query").expect("proxy response");
+
+    assert_eq!(received_rx.recv().expect("query"), b"dns-query");
+    assert_eq!(response, expected_response);
+}
diff --git a/codex-rs/linux-sandbox/src/dns_setup.rs b/codex-rs/linux-sandbox/src/dns_setup.rs
new file mode 100644
index 0000000000..bc6b10bb34
--- /dev/null
+++ b/codex-rs/linux-sandbox/src/dns_setup.rs
@@ -0,0 +1,163 @@
+use crate::bwrap::BwrapArgs;
+use codex_protocol::permissions::ReadDenyMatcher;
+use codex_protocol::protocol::FileSystemSandboxPolicy;
+use rustix::thread::CapabilitySet;
+use rustix::thread::CapabilitySets;
+use rustix::thread::capabilities;
+use rustix::thread::capability_is_in_ambient_set;
+use rustix::thread::capability_is_in_bounding_set;
+use rustix::thread::clear_ambient_capability_set;
+use rustix::thread::remove_capability_from_bounding_set;
+use rustix::thread::set_capabilities;
+use std::fs::File;
+use std::io;
+use std::io::Seek;
+use std::io::SeekFrom;
+use std::io::Write;
+use std::os::fd::AsRawFd;
+use std::os::fd::FromRawFd;
+use std::path::Path;
+use std::path::PathBuf;
+
+const RESOLV_CONF_PATH: &str = "/etc/resolv.conf";
+const LOADER_ENV_KEYS: &[&str] = &["LD_AUDIT", "LD_LIBRARY_PATH", "LD_PRELOAD"];
+
+pub(crate) type LoaderEnvironment = Vec<(String, String)>;
+
+#[derive(Debug)]
+pub(crate) struct ResolvConfMount {
+    pub(crate) file: File,
+    pub(crate) path: PathBuf,
+}
+
+pub(crate) fn create_resolv_conf_file() -> io::Result<File> {
+    let fd = unsafe { libc::memfd_create(c"codex-resolv-conf".as_ptr(), libc::MFD_CLOEXEC) };
+    if fd < 0 {
+        return Err(io::Error::last_os_error());
+    }
+    let mut file = unsafe { File::from_raw_fd(fd) };
+    file.write_all(b"nameserver 127.0.0.1\n")?;
+    file.seek(SeekFrom::Start(0))?;
+    Ok(file)
+}
+
+pub(crate) fn resolv_conf_mount_path(
+    policy: &FileSystemSandboxPolicy,
+    cwd: &Path,
+) -> io::Result<PathBuf> {
+    let logical_path = Path::new(RESOLV_CONF_PATH);
+    let target_path = logical_path.canonicalize()?;
+    ensure_resolver_paths_allowed(policy, cwd, logical_path, &target_path)?;
+    Ok(target_path)
+}
+
+fn ensure_resolver_paths_allowed(
+    policy: &FileSystemSandboxPolicy,
+    cwd: &Path,
+    logical_path: &Path,
+    target_path: &Path,
+) -> io::Result<()> {
+    let deny_matcher = ReadDenyMatcher::new(policy, cwd);
+    if [logical_path, target_path].into_iter().any(|path| {
+        !policy.can_read_path_with_cwd(path, cwd)
+            || deny_matcher
+                .as_ref()
+                .is_some_and(|deny| deny.is_read_denied(path))
+    }) {
+        return Err(io::Error::from(io::ErrorKind::PermissionDenied));
+    }
+    Ok(())
+}
+
+pub(crate) fn capture_loader_environment() -> LoaderEnvironment {
+    LOADER_ENV_KEYS
+        .iter()
+        .filter_map(|&key| {
+            std::env::var_os(key).map(|value| {
+                (
+                    key.to_string(),
+                    value
+                        .into_string()
+                        .unwrap_or_else(|_| panic!("{key} must contain valid UTF-8")),
+                )
+            })
+        })
+        .collect()
+}
+
+pub(crate) fn restore_loader_environment(environment: LoaderEnvironment) {
+    for (key, value) in environment {
+        // SAFETY: the setup process is single-threaded and has dropped all capabilities.
+        unsafe { std::env::set_var(key, value) };
+    }
+}
+
+pub(crate) fn append_bwrap_args(bwrap_args: &mut BwrapArgs, mount: ResolvConfMount) {
+    let separator = bwrap_args
+        .args
+        .iter()
+        .position(|arg| arg == "--")
+        .unwrap_or_else(|| panic!("bubblewrap argv is missing command separator '--'"));
+    let Some(parent) = mount.path.parent() else {
+        panic!("resolver configuration path has no parent");
+    };
+    let fd = mount.file.as_raw_fd().to_string();
+    bwrap_args.args.splice(
+        separator..separator,
+        LOADER_ENV_KEYS
+            .iter()
+            .flat_map(|key| ["--unsetenv".to_string(), (*key).to_string()])
+            .chain([
+                "--cap-drop".to_string(),
+                "ALL".to_string(),
+                "--cap-add".to_string(),
+                "CAP_NET_BIND_SERVICE".to_string(),
+                "--cap-add".to_string(),
+                "CAP_SETPCAP".to_string(),
+                "--dir".to_string(),
+                parent.to_string_lossy().into_owned(),
+                "--perms".to_string(),
+                "444".to_string(),
+                "--ro-bind-data".to_string(),
+                fd,
+                mount.path.to_string_lossy().into_owned(),
+            ]),
+    );
+    bwrap_args.preserved_files.push(mount.file);
+}
+
+pub(crate) fn drop_and_verify_capabilities() -> io::Result<()> {
+    let ignore_unknown = |result: rustix::io::Result<()>| match result {
+        Ok(()) | Err(rustix::io::Errno::INVAL) => Ok(()),
+        Err(err) => Err(io::Error::from_raw_os_error(err.raw_os_error())),
+    };
+    ignore_unknown(clear_ambient_capability_set())?;
+    for bit in 0..u64::BITS {
+        let capability = CapabilitySet::from_bits_retain(1_u64 << bit);
+        match capability_is_in_ambient_set(capability) {
+            Ok(false) | Err(rustix::io::Errno::INVAL) => {}
+            Ok(true) => return Err(io::Error::other("capability remained in ambient set")),
+            Err(err) => return Err(io::Error::from_raw_os_error(err.raw_os_error())),
+        }
+        ignore_unknown(remove_capability_from_bounding_set(capability))?;
+        match capability_is_in_bounding_set(capability) {
+            Ok(false) | Err(rustix::io::Errno::INVAL) => {}
+            Ok(true) => return Err(io::Error::other("capability remained in bounding set")),
+            Err(err) => return Err(io::Error::from_raw_os_error(err.raw_os_error())),
+        }
+    }
+    let empty = CapabilitySets {
+        effective: CapabilitySet::empty(),
+        permitted: CapabilitySet::empty(),
+        inheritable: CapabilitySet::empty(),
+    };
+    set_capabilities(None, empty).map_err(io::Error::from)?;
+    if capabilities(None).map_err(io::Error::from)? != empty {
+        return Err(io::Error::other("capabilities remained after DNS setup"));
+    }
+    Ok(())
+}
+
+#[cfg(test)]
+#[path = "dns_setup_tests.rs"]
+mod tests;
diff --git a/codex-rs/linux-sandbox/src/dns_setup_tests.rs b/codex-rs/linux-sandbox/src/dns_setup_tests.rs
new file mode 100644
index 0000000000..76e5bafe08
--- /dev/null
+++ b/codex-rs/linux-sandbox/src/dns_setup_tests.rs
@@ -0,0 +1,76 @@
+use super::*;
+use crate::bwrap::BwrapArgs;
+use codex_protocol::permissions::FileSystemAccessMode;
+use codex_protocol::permissions::FileSystemPath;
+use codex_protocol::permissions::FileSystemSandboxEntry;
+use codex_protocol::permissions::FileSystemSpecialPath;
+use codex_utils_absolute_path::AbsolutePathBuf;
+use pretty_assertions::assert_eq;
+
+#[test]
+fn unsets_loader_environment_before_inner_command() {
+    let mut bwrap_args = BwrapArgs {
+        args: vec![
+            "bwrap".to_string(),
+            "--".to_string(),
+            "/bin/true".to_string(),
+        ],
+        preserved_files: Vec::new(),
+        synthetic_mount_targets: Vec::new(),
+        protected_create_targets: Vec::new(),
+    };
+    append_bwrap_args(
+        &mut bwrap_args,
+        ResolvConfMount {
+            file: tempfile::tempfile().expect("temporary resolver configuration"),
+            path: PathBuf::from("/etc/resolv.conf"),
+        },
+    );
+
+    let separator = bwrap_args
+        .args
+        .iter()
+        .position(|arg| arg == "--")
+        .expect("command separator");
+    let setup_args = &bwrap_args.args[..separator];
+    for key in ["LD_AUDIT", "LD_LIBRARY_PATH", "LD_PRELOAD"] {
+        assert!(
+            setup_args
+                .windows(2)
+                .any(|args| args == ["--unsetenv", key]),
+            "{key} must be unset before the privileged DNS setup command"
+        );
+    }
+}
+
+#[test]
+fn rejects_read_denied_resolver_paths() {
+    let logical_path = PathBuf::from("/etc/resolv.conf");
+    let target_path = PathBuf::from("/run/systemd/resolve/stub-resolv.conf");
+    for denied_path in [&logical_path, &target_path] {
+        let file_system_sandbox_policy = FileSystemSandboxPolicy::restricted(vec![
+            FileSystemSandboxEntry {
+                path: FileSystemPath::Special {
+                    value: FileSystemSpecialPath::Root,
+                },
+                access: FileSystemAccessMode::Read,
+            },
+            FileSystemSandboxEntry {
+                path: FileSystemPath::Path {
+                    path: AbsolutePathBuf::from_absolute_path(denied_path.clone())
+                        .expect("absolute resolver configuration"),
+                },
+                access: FileSystemAccessMode::Deny,
+            },
+        ]);
+
+        let err = ensure_resolver_paths_allowed(
+            &file_system_sandbox_policy,
+            Path::new("/"),
+            &logical_path,
+            &target_path,
+        )
+        .expect_err("read-denied resolver configuration must be rejected");
+        assert_eq!(err.kind(), std::io::ErrorKind::PermissionDenied);
+    }
+}
diff --git a/codex-rs/linux-sandbox/src/launcher.rs b/codex-rs/linux-sandbox/src/launcher.rs
index 9b80075531..e8a431a842 100644
--- a/codex-rs/linux-sandbox/src/launcher.rs
+++ b/codex-rs/linux-sandbox/src/launcher.rs
@@ -3,6 +3,7 @@ use std::ffi::CString;
 use std::fs::File;
 use std::os::raw::c_char;
 use std::os::unix::ffi::OsStrExt;
+use std::os::unix::fs::PermissionsExt;
 use std::path::Path;
 use std::process::Command;
 use std::sync::OnceLock;
@@ -25,16 +26,19 @@ enum BubblewrapLauncher {
 struct SystemBwrapLauncher {
     program: AbsolutePathBuf,
     supports_argv0: bool,
+    supports_cap_add: bool,
 }
 
 #[derive(Debug, Clone, Copy, PartialEq, Eq)]
 struct SystemBwrapCapabilities {
     supports_argv0: bool,
+    supports_cap_add: bool,
     supports_perms: bool,
+    is_setuid: bool,
 }
 
 pub(crate) fn exec_bwrap(argv: Vec<String>, preserved_files: Vec<File>) -> ! {
-    match preferred_bwrap_launcher() {
+    match preferred_bwrap_launcher_for_argv(&argv) {
         BubblewrapLauncher::System(launcher) => {
             exec_system_bwrap(&launcher.program, argv, preserved_files)
         }
@@ -48,6 +52,13 @@ pub(crate) fn exec_bwrap(argv: Vec<String>, preserved_files: Vec<File>) -> ! {
     }
 }
 
+fn preferred_bwrap_launcher_for_argv(argv: &[String]) -> BubblewrapLauncher {
+    if argv.iter().any(|arg| arg == "--cap-add") {
+        return preferred_bwrap_launcher_supporting_cap_add();
+    }
+    preferred_bwrap_launcher()
+}
+
 fn preferred_bwrap_launcher() -> BubblewrapLauncher {
     static LAUNCHER: OnceLock<BubblewrapLauncher> = OnceLock::new();
     LAUNCHER
@@ -66,6 +77,21 @@ fn preferred_bwrap_launcher() -> BubblewrapLauncher {
         .clone()
 }
 
+fn preferred_bwrap_launcher_supporting_cap_add() -> BubblewrapLauncher {
+    match preferred_bwrap_launcher() {
+        BubblewrapLauncher::System(launcher) if launcher.supports_cap_add => {
+            BubblewrapLauncher::System(launcher)
+        }
+        BubblewrapLauncher::System(_) | BubblewrapLauncher::Unavailable => {
+            match bundled_bwrap::launcher() {
+                Some(launcher) => BubblewrapLauncher::Bundled(launcher),
+                None => BubblewrapLauncher::Unavailable,
+            }
+        }
+        bundled @ BubblewrapLauncher::Bundled(_) => bundled,
+    }
+}
+
 fn system_bwrap_launcher_for_path(system_bwrap_path: &Path) -> Option<SystemBwrapLauncher> {
     system_bwrap_launcher_for_path_with_probe(system_bwrap_path, system_bwrap_capabilities)
 }
@@ -80,7 +106,9 @@ fn system_bwrap_launcher_for_path_with_probe(
 
     let Some(SystemBwrapCapabilities {
         supports_argv0,
+        supports_cap_add,
         supports_perms: true,
+        is_setuid,
     }) = system_bwrap_capabilities(system_bwrap_path)
     else {
         return None;
@@ -95,6 +123,7 @@ fn system_bwrap_launcher_for_path_with_probe(
     Some(SystemBwrapLauncher {
         program: system_bwrap_path,
         supports_argv0,
+        supports_cap_add: supports_cap_add && !is_setuid,
     })
 }
 
@@ -105,6 +134,14 @@ pub(crate) fn preferred_bwrap_supports_argv0() -> bool {
     }
 }
 
+pub(crate) fn preferred_bwrap_supports_cap_add() -> bool {
+    match preferred_bwrap_launcher_supporting_cap_add() {
+        BubblewrapLauncher::System(launcher) => launcher.supports_cap_add,
+        BubblewrapLauncher::Bundled(_) => true,
+        BubblewrapLauncher::Unavailable => false,
+    }
+}
+
 fn system_bwrap_capabilities(system_bwrap_path: &Path) -> Option<SystemBwrapCapabilities> {
     // bubblewrap added `--argv0` in v0.9.0:
     // https://github.com/containers/bubblewrap/releases/tag/v0.9.0
@@ -117,9 +154,12 @@ fn system_bwrap_capabilities(system_bwrap_path: &Path) -> Option<SystemBwrapCapa
     };
     let stdout = String::from_utf8_lossy(&output.stdout);
     let stderr = String::from_utf8_lossy(&output.stderr);
+    let metadata = system_bwrap_path.metadata().ok()?;
     Some(SystemBwrapCapabilities {
         supports_argv0: stdout.contains("--argv0") || stderr.contains("--argv0"),
+        supports_cap_add: stdout.contains("--cap-add") || stderr.contains("--cap-add"),
         supports_perms: stdout.contains("--perms") || stderr.contains("--perms"),
+        is_setuid: metadata.permissions().mode() & libc::S_ISUID != 0,
     })
 }
 
@@ -167,12 +207,15 @@ mod tests {
             system_bwrap_launcher_for_path_with_probe(fake_bwrap_path, |_| {
                 Some(SystemBwrapCapabilities {
                     supports_argv0: true,
+                    supports_cap_add: false,
                     supports_perms: true,
+                    is_setuid: false,
                 })
             }),
             Some(SystemBwrapLauncher {
                 program: expected,
                 supports_argv0: true,
+                supports_cap_add: false,
             })
         );
     }
@@ -186,12 +229,15 @@ mod tests {
             system_bwrap_launcher_for_path_with_probe(fake_bwrap_path, |_| {
                 Some(SystemBwrapCapabilities {
                     supports_argv0: false,
+                    supports_cap_add: false,
                     supports_perms: true,
+                    is_setuid: false,
                 })
             }),
             Some(SystemBwrapLauncher {
                 program: AbsolutePathBuf::from_absolute_path(fake_bwrap_path).expect("absolute"),
                 supports_argv0: false,
+                supports_cap_add: false,
             })
         );
     }
@@ -204,13 +250,34 @@ mod tests {
             system_bwrap_launcher_for_path_with_probe(fake_bwrap.path(), |_| {
                 Some(SystemBwrapCapabilities {
                     supports_argv0: false,
+                    supports_cap_add: false,
                     supports_perms: false,
+                    is_setuid: false,
                 })
             }),
             None
         );
     }
 
+    #[test]
+    fn disables_system_cap_add_when_system_bwrap_is_setuid() {
+        let fake_bwrap = NamedTempFile::new().expect("temp file");
+
+        assert_eq!(
+            system_bwrap_launcher_for_path_with_probe(fake_bwrap.path(), |_| {
+                Some(SystemBwrapCapabilities {
+                    supports_argv0: true,
+                    supports_cap_add: true,
+                    supports_perms: true,
+                    is_setuid: true,
+                })
+            })
+            .expect("system launcher")
+            .supports_cap_add,
+            false
+        );
+    }
+
     #[test]
     fn ignores_system_bwrap_when_system_bwrap_is_missing() {
         assert_eq!(
diff --git a/codex-rs/linux-sandbox/src/lib.rs b/codex-rs/linux-sandbox/src/lib.rs
index 478cd6c379..488ff40e60 100644
--- a/codex-rs/linux-sandbox/src/lib.rs
+++ b/codex-rs/linux-sandbox/src/lib.rs
@@ -10,6 +10,10 @@ mod bundled_bwrap;
 #[cfg(target_os = "linux")]
 mod bwrap;
 #[cfg(target_os = "linux")]
+mod dns_routing;
+#[cfg(target_os = "linux")]
+mod dns_setup;
+#[cfg(target_os = "linux")]
 mod exec_util;
 #[cfg(target_os = "linux")]
 mod landlock;
diff --git a/codex-rs/linux-sandbox/src/linux_run_main.rs b/codex-rs/linux-sandbox/src/linux_run_main.rs
index 346b1f14c0..b4c53dc359 100644
--- a/codex-rs/linux-sandbox/src/linux_run_main.rs
+++ b/codex-rs/linux-sandbox/src/linux_run_main.rs
@@ -20,11 +20,23 @@ use std::time::Duration;
 use crate::bwrap::BwrapNetworkMode;
 use crate::bwrap::BwrapOptions;
 use crate::bwrap::create_bwrap_command_args;
+use crate::dns_routing::bind_netns_dns_stub;
+use crate::dns_routing::spawn_netns_dns_stub;
+use crate::dns_setup::LoaderEnvironment;
+use crate::dns_setup::ResolvConfMount;
+use crate::dns_setup::append_bwrap_args as append_dns_bwrap_args;
+use crate::dns_setup::capture_loader_environment;
+use crate::dns_setup::create_resolv_conf_file;
+use crate::dns_setup::drop_and_verify_capabilities;
+use crate::dns_setup::resolv_conf_mount_path;
+use crate::dns_setup::restore_loader_environment;
 use crate::landlock::apply_permission_profile_to_current_thread;
 use crate::launcher::exec_bwrap;
 use crate::launcher::preferred_bwrap_supports_argv0;
+use crate::launcher::preferred_bwrap_supports_cap_add;
 use crate::proxy_routing::activate_proxy_routes_in_netns;
 use crate::proxy_routing::prepare_host_proxy_route_spec;
+use codex_network_proxy::DNS_PROXY_ENV_KEY;
 use codex_protocol::error::Result as CodexResult;
 use codex_protocol::models::PermissionProfile;
 use codex_protocol::protocol::FileSystemSandboxPolicy;
@@ -126,6 +138,10 @@ pub struct LandlockCommand {
     #[arg(long = "proxy-route-spec", hide = true)]
     pub proxy_route_spec: Option<String>,
 
+    /// Internal loader environment restored after temporary DNS setup capabilities are dropped.
+    #[arg(long = "loader-environment", hide = true)]
+    pub loader_environment: Option<String>,
+
     /// When set, skip mounting a fresh `/proc` even though PID isolation is
     /// still enabled. This is primarily intended for restrictive container
     /// environments that deny `--proc /proc`.
@@ -153,6 +169,7 @@ pub fn run_main() -> ! {
         apply_seccomp_then_exec,
         allow_network_for_proxy,
         proxy_route_spec,
+        loader_environment,
         no_proc,
         command,
     } = LandlockCommand::parse();
@@ -177,12 +194,35 @@ pub fn run_main() -> ! {
     // established the filesystem view.
     if apply_seccomp_then_exec {
         if allow_network_for_proxy {
+            let bound_dns = if std::env::var_os(DNS_PROXY_ENV_KEY).is_some() {
+                Some(
+                    bind_netns_dns_stub()
+                        .unwrap_or_else(|err| panic!("error binding Linux DNS bridge: {err}")),
+                )
+            } else {
+                None
+            };
+            let loader_environment = parse_loader_environment(loader_environment.as_deref())
+                .unwrap_or_else(|err| panic!("invalid loader environment: {err}"));
+            if bound_dns.is_some() {
+                drop_and_verify_capabilities().unwrap_or_else(|err| {
+                    panic!("error dropping Linux DNS setup capabilities: {err}")
+                });
+                if let Some(loader_environment) = loader_environment {
+                    restore_loader_environment(loader_environment);
+                }
+            }
             let spec = proxy_route_spec
                 .as_deref()
                 .unwrap_or_else(|| panic!("managed proxy mode requires --proxy-route-spec"));
             if let Err(err) = activate_proxy_routes_in_netns(spec) {
                 panic!("error activating Linux proxy routing bridge: {err}");
             }
+            if let Some(bound_dns) = bound_dns
+                && let Err(err) = spawn_netns_dns_stub(bound_dns)
+            {
+                panic!("error activating Linux DNS bridge: {err}");
+            }
         }
         let proxy_routing_active = allow_network_for_proxy;
         if let Err(e) = apply_permission_profile_to_current_thread(
@@ -214,6 +254,11 @@ pub fn run_main() -> ! {
         // Outer stage: bubblewrap first, then re-enter this binary in the
         // sandboxed environment to apply seccomp. This path never falls back
         // to legacy Landlock on failure.
+        let dns_setup = prepare_dns_setup(
+            allow_network_for_proxy,
+            &file_system_sandbox_policy,
+            &sandbox_policy_cwd,
+        );
         let proxy_route_spec =
             if allow_network_for_proxy {
                 Some(prepare_host_proxy_route_spec().unwrap_or_else(|err| {
@@ -228,6 +273,9 @@ pub fn run_main() -> ! {
             permission_profile: &permission_profile,
             allow_network_for_proxy,
             proxy_route_spec,
+            loader_environment: dns_setup
+                .as_ref()
+                .map(|setup| serialize_loader_environment(&setup.loader_environment)),
             command,
         });
         run_bwrap_with_proc_fallback(
@@ -238,6 +286,7 @@ pub fn run_main() -> ! {
             inner,
             !no_proc,
             allow_network_for_proxy,
+            dns_setup.map(|setup| setup.resolv_conf),
         );
     }
 
@@ -254,6 +303,11 @@ pub fn run_main() -> ! {
     exec_or_panic(command);
 }
 
+struct DnsSetup {
+    resolv_conf: ResolvConfMount,
+    loader_environment: LoaderEnvironment,
+}
+
 #[derive(Debug, Clone)]
 struct EffectivePermissions {
     permission_profile: PermissionProfile,
@@ -278,6 +332,45 @@ fn parse_permission_profile(value: &str) -> std::result::Result<PermissionProfil
     serde_json::from_str(value).map_err(|err| format!("invalid permission profile JSON: {err}"))
 }
 
+fn parse_loader_environment(
+    value: Option<&str>,
+) -> std::result::Result<Option<LoaderEnvironment>, String> {
+    value
+        .map(serde_json::from_str)
+        .transpose()
+        .map_err(|err| format!("invalid loader environment JSON: {err}"))
+}
+
+fn serialize_loader_environment(environment: &LoaderEnvironment) -> String {
+    serde_json::to_string(environment)
+        .unwrap_or_else(|err| panic!("failed to serialize loader environment: {err}"))
+}
+
+fn prepare_dns_setup(
+    allow_network_for_proxy: bool,
+    file_system_sandbox_policy: &FileSystemSandboxPolicy,
+    sandbox_policy_cwd: &Path,
+) -> Option<DnsSetup> {
+    if !allow_network_for_proxy || std::env::var_os(DNS_PROXY_ENV_KEY).is_none() {
+        return None;
+    }
+    if !preferred_bwrap_supports_cap_add() {
+        // SAFETY: the sandbox helper is single-threaded here, before it forks bridge workers or
+        // executes the user command.
+        unsafe { std::env::remove_var(DNS_PROXY_ENV_KEY) };
+        return None;
+    }
+    Some(DnsSetup {
+        resolv_conf: ResolvConfMount {
+            file: create_resolv_conf_file()
+                .unwrap_or_else(|err| panic!("failed to create resolver configuration: {err}")),
+            path: resolv_conf_mount_path(file_system_sandbox_policy, sandbox_policy_cwd)
+                .unwrap_or_else(|err| panic!("failed to prepare resolver configuration: {err}")),
+        },
+        loader_environment: capture_loader_environment(),
+    })
+}
+
 fn resolve_permission_profile(
     permission_profile: Option<PermissionProfile>,
 ) -> Result<EffectivePermissions, ResolvePermissionProfileError> {
@@ -322,6 +415,7 @@ fn run_bwrap_with_proc_fallback(
     inner: Vec<String>,
     mount_proc: bool,
     allow_network_for_proxy: bool,
+    dns_resolv_conf: Option<ResolvConfMount>,
 ) -> ! {
     let network_mode = bwrap_network_mode(network_sandbox_policy, allow_network_for_proxy);
     let mut mount_proc = mount_proc;
@@ -354,6 +448,9 @@ fn run_bwrap_with_proc_fallback(
         options,
     )
     .unwrap_or_else(|err| exit_with_bwrap_build_error(err));
+    if let Some(dns_resolv_conf) = dns_resolv_conf {
+        append_dns_bwrap_args(&mut bwrap_args, dns_resolv_conf);
+    }
     apply_inner_command_argv0(&mut bwrap_args.args);
     run_or_exec_bwrap(bwrap_args);
 }
@@ -1394,6 +1491,7 @@ struct InnerSeccompCommandArgs<'a> {
     permission_profile: &'a PermissionProfile,
     allow_network_for_proxy: bool,
     proxy_route_spec: Option<String>,
+    loader_environment: Option<String>,
     command: Vec<String>,
 }
 
@@ -1405,6 +1503,7 @@ fn build_inner_seccomp_command(args: InnerSeccompCommandArgs<'_>) -> Vec<String>
         permission_profile,
         allow_network_for_proxy,
         proxy_route_spec,
+        loader_environment,
         command,
     } = args;
     let current_exe = match std::env::current_exe() {
@@ -1436,6 +1535,10 @@ fn build_inner_seccomp_command(args: InnerSeccompCommandArgs<'_>) -> Vec<String>
             .unwrap_or_else(|| panic!("managed proxy mode requires a proxy route spec"));
         inner.push("--proxy-route-spec".to_string());
         inner.push(proxy_route_spec);
+        if let Some(loader_environment) = loader_environment {
+            inner.push("--loader-environment".to_string());
+            inner.push(loader_environment);
+        }
     }
     inner.push("--".to_string());
     inner.extend(command);
diff --git a/codex-rs/linux-sandbox/src/linux_run_main_tests.rs b/codex-rs/linux-sandbox/src/linux_run_main_tests.rs
index 4441af7809..e54b57cb18 100644
--- a/codex-rs/linux-sandbox/src/linux_run_main_tests.rs
+++ b/codex-rs/linux-sandbox/src/linux_run_main_tests.rs
@@ -468,6 +468,7 @@ fn managed_proxy_inner_command_includes_route_spec() {
         permission_profile: &permission_profile,
         allow_network_for_proxy: true,
         proxy_route_spec: Some("{\"routes\":[]}".to_string()),
+        loader_environment: None,
         command: vec!["/bin/true".to_string()],
     });
 
@@ -484,6 +485,7 @@ fn inner_command_includes_permission_profile_flag() {
         permission_profile: &permission_profile,
         allow_network_for_proxy: false,
         proxy_route_spec: None,
+        loader_environment: None,
         command: vec!["/bin/true".to_string()],
     });
 
@@ -503,6 +505,7 @@ fn non_managed_inner_command_omits_route_spec() {
         permission_profile: &permission_profile,
         allow_network_for_proxy: false,
         proxy_route_spec: None,
+        loader_environment: None,
         command: vec!["/bin/true".to_string()],
     });
 
@@ -519,6 +522,7 @@ fn managed_proxy_inner_command_requires_route_spec() {
             permission_profile: &permission_profile,
             allow_network_for_proxy: true,
             proxy_route_spec: None,
+            loader_environment: None,
             command: vec!["/bin/true".to_string()],
         })
     });
diff --git a/codex-rs/linux-sandbox/src/proxy_routing.rs b/codex-rs/linux-sandbox/src/proxy_routing.rs
index 707cbaafbe..be3217875e 100644
--- a/codex-rs/linux-sandbox/src/proxy_routing.rs
+++ b/codex-rs/linux-sandbox/src/proxy_routing.rs
@@ -1,3 +1,4 @@
+use codex_network_proxy::DNS_PROXY_ENV_KEY;
 use codex_network_proxy::PROXY_ATTRIBUTION_TOKEN_ENV_KEY;
 use codex_network_proxy::write_attribution_frame;
 use serde::Deserialize;
@@ -41,6 +42,7 @@ const PROXY_ENV_KEYS: &[&str] = &[
     "PIP_PROXY",
     "DOCKER_HTTP_PROXY",
     "DOCKER_HTTPS_PROXY",
+    DNS_PROXY_ENV_KEY,
 ];
 
 const PROXY_SOCKET_DIR_PREFIX: &str = "codex-linux-sandbox-proxy-";
@@ -672,7 +674,7 @@ fn set_parent_death_signal() -> io::Result<()> {
     }
 }
 
-fn harden_bridge_process() -> io::Result<()> {
+pub(crate) fn harden_bridge_process() -> io::Result<()> {
     set_parent_death_signal()?;
     codex_process_hardening::disable_process_dumping()
 }
diff --git a/codex-rs/linux-sandbox/tests/suite/managed_proxy.rs b/codex-rs/linux-sandbox/tests/suite/managed_proxy.rs
index 6c9a6a0c67..3f34f627a9 100644
--- a/codex-rs/linux-sandbox/tests/suite/managed_proxy.rs
+++ b/codex-rs/linux-sandbox/tests/suite/managed_proxy.rs
@@ -2,6 +2,8 @@
 #![allow(clippy::unwrap_used)]
 
 use codex_core::exec_env::create_env;
+use codex_network_proxy::DNS_PROXY_ENV_KEY;
+use codex_network_proxy::DNS_PROXY_SESSION_PREFACE;
 use codex_protocol::config_types::ShellEnvironmentPolicy;
 use codex_protocol::models::PermissionProfile;
 use pretty_assertions::assert_eq;
@@ -40,6 +42,7 @@ const PROXY_ENV_KEYS: &[&str] = &[
     "PIP_PROXY",
     "DOCKER_HTTP_PROXY",
     "DOCKER_HTTPS_PROXY",
+    DNS_PROXY_ENV_KEY,
 ];
 
 fn create_env_from_core_vars() -> HashMap<String, String> {
@@ -301,3 +304,142 @@ async fn managed_proxy_mode_denies_af_unix_socket_but_allows_socketpair() {
         String::from_utf8_lossy(&output.stderr)
     );
 }
+
+#[tokio::test]
+async fn managed_proxy_mode_routes_native_dns_through_bridge() {
+    if let Some(skip_reason) = managed_proxy_skip_reason().await {
+        eprintln!("skipping managed proxy test: {skip_reason}");
+        return;
+    }
+
+    if !command_available("python3").await {
+        eprintln!("skipping managed proxy DNS test: python3 is unavailable");
+        return;
+    }
+
+    let listener = TcpListener::bind((Ipv4Addr::LOCALHOST, 0)).expect("bind DNS proxy listener");
+    let proxy_port = listener.local_addr().expect("DNS proxy local addr").port();
+    let (query_tx, query_rx) = std::sync::mpsc::channel();
+    std::thread::spawn(move || {
+        let (mut stream, _) = listener.accept().expect("accept DNS proxy connection");
+        stream
+            .set_read_timeout(Some(Duration::from_secs(3)))
+            .expect("set DNS proxy read timeout");
+        let mut preface = [0_u8; DNS_PROXY_SESSION_PREFACE.len()];
+        stream.read_exact(&mut preface).expect("read DNS preface");
+        assert_eq!(&preface, DNS_PROXY_SESSION_PREFACE);
+        stream
+            .write_all(DNS_PROXY_SESSION_PREFACE)
+            .expect("write DNS preface ack");
+        let query = read_frame(&mut stream).expect("read DNS query");
+        let response = dns_a_response(&query, [203, 0, 113, 9]);
+        query_tx.send(query).expect("send DNS query");
+        write_frame(&mut stream, &response).expect("write DNS response");
+    });
+
+    let mut env = create_env_from_core_vars();
+    strip_proxy_env(&mut env);
+    env.insert(
+        DNS_PROXY_ENV_KEY.to_string(),
+        format!("tcp://127.0.0.1:{proxy_port}"),
+    );
+
+    let output = run_linux_sandbox_direct(
+        &[
+            "python3",
+            "-c",
+            "import os,socket,sys\nif 'CODEX_NETWORK_PROXY_DNS' in os.environ:\n    sys.exit(3)\ninfo = socket.getaddrinfo('fixture.test', 80, socket.AF_INET, socket.SOCK_STREAM)\nprint(info[0][4][0])\n",
+        ],
+        &PermissionProfile::Disabled,
+        /*allow_network_for_proxy*/ true,
+        env,
+        NETWORK_TIMEOUT_MS,
+    )
+    .await;
+
+    assert_eq!(
+        output.status.success(),
+        true,
+        "expected native DNS to resolve through bridge; status={:?}; stdout={}; stderr={}",
+        output.status.code(),
+        String::from_utf8_lossy(&output.stdout),
+        String::from_utf8_lossy(&output.stderr)
+    );
+    assert_eq!(
+        String::from_utf8_lossy(&output.stdout).trim(),
+        "203.0.113.9"
+    );
+    let query = query_rx
+        .recv_timeout(Duration::from_secs(3))
+        .expect("expected DNS query through proxy bridge");
+    assert!(
+        dns_query_name(&query).is_some_and(|name| name == "fixture.test"),
+        "expected fixture.test DNS query, got wire bytes: {query:?}"
+    );
+}
+
+fn dns_query_name(query: &[u8]) -> Option<String> {
+    let mut offset = 12usize;
+    let mut labels = Vec::new();
+    loop {
+        let len = *query.get(offset)? as usize;
+        offset += 1;
+        if len == 0 {
+            break;
+        }
+        let label = query.get(offset..offset.checked_add(len)?)?;
+        labels.push(std::str::from_utf8(label).ok()?);
+        offset += len;
+    }
+    Some(labels.join("."))
+}
+
+fn dns_a_response(query: &[u8], address: [u8; 4]) -> Vec<u8> {
+    let question_end = dns_question_end(query).expect("DNS question end");
+    let mut response = Vec::new();
+    response.extend_from_slice(&query[..2]);
+    response.extend_from_slice(&[0x81, 0x80]);
+    response.extend_from_slice(&[0x00, 0x01]);
+    response.extend_from_slice(&[0x00, 0x01]);
+    response.extend_from_slice(&[0x00, 0x00]);
+    response.extend_from_slice(&[0x00, 0x00]);
+    response.extend_from_slice(&query[12..question_end]);
+    response.extend_from_slice(&[0xc0, 0x0c]);
+    response.extend_from_slice(&[0x00, 0x01]);
+    response.extend_from_slice(&[0x00, 0x01]);
+    response.extend_from_slice(&[0x00, 0x00, 0x00, 0x00]);
+    response.extend_from_slice(&[0x00, 0x04]);
+    response.extend_from_slice(&address);
+    response
+}
+
+fn dns_question_end(query: &[u8]) -> Option<usize> {
+    let mut offset = 12usize;
+    loop {
+        let len = *query.get(offset)? as usize;
+        offset += 1;
+        if len == 0 {
+            return offset.checked_add(4).filter(|end| *end <= query.len());
+        }
+        offset = offset.checked_add(len)?;
+    }
+}
+
+fn write_frame(writer: &mut impl Write, payload: &[u8]) -> std::io::Result<()> {
+    let len = u16::try_from(payload.len()).map_err(|_| {
+        std::io::Error::new(
+            std::io::ErrorKind::InvalidInput,
+            "DNS message exceeds maximum wire length",
+        )
+    })?;
+    writer.write_all(&len.to_be_bytes())?;
+    writer.write_all(payload)
+}
+
+fn read_frame(reader: &mut impl Read) -> std::io::Result<Vec<u8>> {
+    let mut len = [0; 2];
+    reader.read_exact(&mut len)?;
+    let mut payload = vec![0; usize::from(u16::from_be_bytes(len))];
+    reader.read_exact(&mut payload)?;
+    Ok(payload)
+}