diff --git a/codex-rs/app-server/BUILD.bazel b/codex-rs/app-server/BUILD.bazel
index 5f1ba790d5..e18721fa09 100644
--- a/codex-rs/app-server/BUILD.bazel
+++ b/codex-rs/app-server/BUILD.bazel
@@ -3,5 +3,8 @@ load("//:defs.bzl", "codex_rust_crate")
 codex_rust_crate(
     name = "app-server",
     crate_name = "codex_app_server",
+    extra_binaries = [
+        "//codex-rs/rmcp-client:test_stdio_server",
+    ],
     test_tags = ["no-sandbox"],
 )
diff --git a/codex-rs/app-server/src/codex_message_processor.rs b/codex-rs/app-server/src/codex_message_processor.rs
index c70be7e8e9..4fc4916ad9 100644
--- a/codex-rs/app-server/src/codex_message_processor.rs
+++ b/codex-rs/app-server/src/codex_message_processor.rs
@@ -3272,9 +3272,14 @@ impl CodexMessageProcessor {
         self.command_exec_manager
             .connection_closed(connection_id)
             .await;
-        self.thread_state_manager
+        let orphaned_thread_ids = self
+            .thread_state_manager
             .remove_connection(connection_id)
             .await;
+        for thread_id in orphaned_thread_ids {
+            self.maybe_unload_orphaned_thread_after_disconnect(thread_id)
+                .await;
+        }
     }
 
     pub(crate) fn subscribe_running_assistant_turn_count(&self) -> watch::Receiver<usize> {
@@ -4834,6 +4839,93 @@ impl CodexMessageProcessor {
         }
     }
 
+    fn should_unload_orphaned_thread_after_disconnect(
+        rollout_path: Option<&Path>,
+        agent_status: AgentStatus,
+        loaded_status: ThreadStatus,
+    ) -> bool {
+        rollout_path.is_some_and(std::path::Path::exists)
+            && !matches!(agent_status, AgentStatus::Running)
+            && matches!(
+                loaded_status,
+                ThreadStatus::Idle | ThreadStatus::SystemError
+            )
+    }
+
+    async fn begin_thread_shutdown(&self, thread_id: ThreadId, thread: Arc<CodexThread>) {
+        info!("thread {thread_id} has no subscribers; shutting down");
+        self.pending_thread_unloads.lock().await.insert(thread_id);
+        // Any pending app-server -> client requests for this thread can no longer be
+        // answered; cancel their callbacks before shutdown/unload.
+        self.outgoing
+            .cancel_requests_for_thread(thread_id, None)
+            .await;
+        self.thread_state_manager
+            .remove_thread_state(thread_id)
+            .await;
+
+        let outgoing = self.outgoing.clone();
+        let pending_thread_unloads = self.pending_thread_unloads.clone();
+        let thread_manager = self.thread_manager.clone();
+        let thread_watch_manager = self.thread_watch_manager.clone();
+        tokio::spawn(async move {
+            match Self::wait_for_thread_shutdown(&thread).await {
+                ThreadShutdownResult::Complete => {
+                    if thread_manager.remove_thread(&thread_id).await.is_none() {
+                        info!("thread {thread_id} was already removed before shutdown finalized");
+                        thread_watch_manager
+                            .remove_thread(&thread_id.to_string())
+                            .await;
+                        pending_thread_unloads.lock().await.remove(&thread_id);
+                        return;
+                    }
+                    thread_watch_manager
+                        .remove_thread(&thread_id.to_string())
+                        .await;
+                    let notification = ThreadClosedNotification {
+                        thread_id: thread_id.to_string(),
+                    };
+                    outgoing
+                        .send_server_notification(ServerNotification::ThreadClosed(notification))
+                        .await;
+                    pending_thread_unloads.lock().await.remove(&thread_id);
+                }
+                ThreadShutdownResult::SubmitFailed => {
+                    pending_thread_unloads.lock().await.remove(&thread_id);
+                    warn!("failed to submit Shutdown to thread {thread_id}");
+                }
+                ThreadShutdownResult::TimedOut => {
+                    pending_thread_unloads.lock().await.remove(&thread_id);
+                    warn!("thread {thread_id} shutdown timed out; leaving thread loaded");
+                }
+            }
+        });
+    }
+
+    async fn maybe_unload_orphaned_thread_after_disconnect(&self, thread_id: ThreadId) {
+        let Ok(thread) = self.thread_manager.get_thread(thread_id).await else {
+            return;
+        };
+
+        let loaded_status = self
+            .thread_watch_manager
+            .loaded_status_for_thread(&thread_id.to_string())
+            .await;
+        let agent_status = thread.agent_status().await;
+        if !Self::should_unload_orphaned_thread_after_disconnect(
+            thread.rollout_path().as_deref(),
+            agent_status,
+            loaded_status,
+        ) {
+            return;
+        }
+        if self.thread_state_manager.has_subscribers(thread_id).await {
+            return;
+        }
+
+        self.begin_thread_shutdown(thread_id, thread).await;
+    }
+
     async fn finalize_thread_teardown(&mut self, thread_id: ThreadId) {
         self.pending_thread_unloads.lock().await.remove(&thread_id);
         self.outgoing
@@ -4895,57 +4987,7 @@ impl CodexMessageProcessor {
 
         if !self.thread_state_manager.has_subscribers(thread_id).await {
             // This connection was the last subscriber. Only now do we unload the thread.
-            info!("thread {thread_id} has no subscribers; shutting down");
-            self.pending_thread_unloads.lock().await.insert(thread_id);
-            // Any pending app-server -> client requests for this thread can no longer be
-            // answered; cancel their callbacks before shutdown/unload.
-            self.outgoing
-                .cancel_requests_for_thread(thread_id, /*error*/ None)
-                .await;
-            self.thread_state_manager
-                .remove_thread_state(thread_id)
-                .await;
-
-            let outgoing = self.outgoing.clone();
-            let pending_thread_unloads = self.pending_thread_unloads.clone();
-            let thread_manager = self.thread_manager.clone();
-            let thread_watch_manager = self.thread_watch_manager.clone();
-            tokio::spawn(async move {
-                match Self::wait_for_thread_shutdown(&thread).await {
-                    ThreadShutdownResult::Complete => {
-                        if thread_manager.remove_thread(&thread_id).await.is_none() {
-                            info!(
-                                "thread {thread_id} was already removed before unsubscribe finalized"
-                            );
-                            thread_watch_manager
-                                .remove_thread(&thread_id.to_string())
-                                .await;
-                            pending_thread_unloads.lock().await.remove(&thread_id);
-                            return;
-                        }
-                        thread_watch_manager
-                            .remove_thread(&thread_id.to_string())
-                            .await;
-                        let notification = ThreadClosedNotification {
-                            thread_id: thread_id.to_string(),
-                        };
-                        outgoing
-                            .send_server_notification(ServerNotification::ThreadClosed(
-                                notification,
-                            ))
-                            .await;
-                        pending_thread_unloads.lock().await.remove(&thread_id);
-                    }
-                    ThreadShutdownResult::SubmitFailed => {
-                        pending_thread_unloads.lock().await.remove(&thread_id);
-                        warn!("failed to submit Shutdown to thread {thread_id}");
-                    }
-                    ThreadShutdownResult::TimedOut => {
-                        pending_thread_unloads.lock().await.remove(&thread_id);
-                        warn!("thread {thread_id} shutdown timed out; leaving thread loaded");
-                    }
-                }
-            });
+            self.begin_thread_shutdown(thread_id, thread).await;
         }
 
         self.outgoing
@@ -8598,12 +8640,13 @@ mod tests {
             state.lock().await.cancel_tx = Some(cancel_tx);
         }
 
-        manager.remove_connection(connection_a).await;
+        let orphaned_thread_ids = manager.remove_connection(connection_a).await;
         assert!(
             tokio::time::timeout(Duration::from_millis(20), &mut cancel_rx)
                 .await
                 .is_err()
         );
+        assert!(orphaned_thread_ids.is_empty());
 
         assert_eq!(
             manager.subscribed_connection_ids(thread_id).await,
@@ -8612,6 +8655,25 @@ mod tests {
         Ok(())
     }
 
+    #[tokio::test]
+    async fn removing_last_connection_reports_orphaned_thread() -> Result<()> {
+        let manager = ThreadStateManager::new();
+        let thread_id = ThreadId::from_string("ad7f0408-99b8-4f6e-a46f-bd0eec433370")?;
+        let connection = ConnectionId(1);
+
+        manager.connection_initialized(connection).await;
+        manager
+            .try_ensure_connection_subscribed(thread_id, connection, false)
+            .await
+            .expect("connection should be live");
+
+        let orphaned_thread_ids = manager.remove_connection(connection).await;
+
+        assert_eq!(orphaned_thread_ids, vec![thread_id]);
+        assert!(!manager.has_subscribers(thread_id).await);
+        Ok(())
+    }
+
     #[tokio::test]
     async fn closed_connection_cannot_be_reintroduced_by_auto_subscribe() -> Result<()> {
         let manager = ThreadStateManager::new();
@@ -8619,7 +8681,8 @@ mod tests {
         let connection = ConnectionId(1);
 
         manager.connection_initialized(connection).await;
-        manager.remove_connection(connection).await;
+        let orphaned_thread_ids = manager.remove_connection(connection).await;
+        assert!(orphaned_thread_ids.is_empty());
 
         assert!(
             manager
diff --git a/codex-rs/app-server/src/thread_state.rs b/codex-rs/app-server/src/thread_state.rs
index be5478dd51..8f7cb5fa24 100644
--- a/codex-rs/app-server/src/thread_state.rs
+++ b/codex-rs/app-server/src/thread_state.rs
@@ -313,8 +313,8 @@ impl ThreadStateManager {
         true
     }
 
-    pub(crate) async fn remove_connection(&self, connection_id: ConnectionId) {
-        let thread_states = {
+    pub(crate) async fn remove_connection(&self, connection_id: ConnectionId) -> Vec<ThreadId> {
+        let orphaned_threads = {
             let mut state = self.state.lock().await;
             state.live_connections.remove(&connection_id);
             let thread_ids = state
@@ -344,7 +344,9 @@ impl ThreadStateManager {
                 .collect::<Vec<_>>()
         };
 
-        for (thread_id, no_subscribers, thread_state) in thread_states {
+        let mut orphaned_thread_ids = Vec::new();
+
+        for (thread_id, no_subscribers, thread_state) in orphaned_threads {
             if !no_subscribers {
                 continue;
             }
@@ -358,6 +360,9 @@ impl ThreadStateManager {
                 listener_generation,
                 "retaining thread listener after connection disconnect left zero subscribers"
             );
+            orphaned_thread_ids.push(thread_id);
         }
+
+        orphaned_thread_ids
     }
 }
diff --git a/codex-rs/app-server/tests/suite/v2/mod.rs b/codex-rs/app-server/tests/suite/v2/mod.rs
index 7fa5520a23..f33589d9fe 100644
--- a/codex-rs/app-server/tests/suite/v2/mod.rs
+++ b/codex-rs/app-server/tests/suite/v2/mod.rs
@@ -30,6 +30,8 @@ mod review;
 mod safety_check_downgrade;
 mod skills_list;
 mod thread_archive;
+#[cfg(unix)]
+mod thread_disconnect_websocket_unix;
 mod thread_fork;
 mod thread_list;
 mod thread_loaded_list;
diff --git a/codex-rs/app-server/tests/suite/v2/thread_disconnect_websocket_unix.rs b/codex-rs/app-server/tests/suite/v2/thread_disconnect_websocket_unix.rs
new file mode 100644
index 0000000000..a468e50ecf
--- /dev/null
+++ b/codex-rs/app-server/tests/suite/v2/thread_disconnect_websocket_unix.rs
@@ -0,0 +1,245 @@
+use super::connection_handling_websocket::DEFAULT_READ_TIMEOUT;
+use super::connection_handling_websocket::WsClient;
+use super::connection_handling_websocket::connect_websocket;
+use super::connection_handling_websocket::create_config_toml;
+use super::connection_handling_websocket::read_response_for_id;
+use super::connection_handling_websocket::send_initialize_request;
+use super::connection_handling_websocket::send_request;
+use super::connection_handling_websocket::spawn_websocket_server;
+use anyhow::Context;
+use anyhow::Result;
+use app_test_support::create_fake_rollout_with_text_elements;
+use app_test_support::create_mock_responses_server_repeating_assistant;
+use app_test_support::to_response;
+use codex_app_server_protocol::JSONRPCResponse;
+use codex_app_server_protocol::ThreadLoadedListParams;
+use codex_app_server_protocol::ThreadLoadedListResponse;
+use codex_app_server_protocol::ThreadResumeParams;
+use codex_app_server_protocol::ThreadResumeResponse;
+use core_test_support::stdio_server_bin;
+use pretty_assertions::assert_eq;
+use std::os::unix::fs::PermissionsExt;
+use std::path::Path;
+use std::process::Command;
+use tempfile::TempDir;
+use tokio::time::Duration;
+use tokio::time::sleep;
+use tokio::time::timeout;
+
+fn process_is_running(pid: u32) -> bool {
+    let output = Command::new("ps")
+        .args(["-o", "stat=", "-p", &pid.to_string()])
+        .stderr(std::process::Stdio::null())
+        .output();
+
+    output
+        .ok()
+        .filter(|output| output.status.success())
+        .and_then(|output| {
+            String::from_utf8_lossy(&output.stdout)
+                .lines()
+                .find_map(|line| {
+                    let trimmed = line.trim();
+                    (!trimmed.is_empty()).then_some(trimmed.to_owned())
+                })
+        })
+        .is_some_and(|stat| !stat.starts_with('Z'))
+}
+
+async fn wait_for_pid_entry(path: &Path) -> Result<u32> {
+    for _ in 0..50 {
+        match std::fs::read_to_string(path) {
+            Ok(content) => {
+                let Some(pid) = content
+                    .lines()
+                    .find_map(|line| {
+                        let trimmed = line.trim();
+                        (!trimmed.is_empty()).then_some(trimmed)
+                    })
+                    .map(str::parse::<u32>)
+                    .transpose()
+                    .with_context(|| format!("failed to parse pid from {}", path.display()))?
+                else {
+                    sleep(Duration::from_millis(100)).await;
+                    continue;
+                };
+                return Ok(pid);
+            }
+            Err(error) if error.kind() == std::io::ErrorKind::NotFound => {
+                sleep(Duration::from_millis(100)).await;
+            }
+            Err(error) => {
+                return Err(error).with_context(|| format!("failed to read {}", path.display()));
+            }
+        }
+    }
+
+    anyhow::bail!("timed out waiting for pid file at {}", path.display());
+}
+
+async fn wait_for_process_exit(pid: u32) -> Result<()> {
+    for _ in 0..50 {
+        if !process_is_running(pid) {
+            return Ok(());
+        }
+        sleep(Duration::from_millis(100)).await;
+    }
+
+    anyhow::bail!("process {pid} still running after timeout");
+}
+
+fn ensure_stdio_server_bin() -> Result<String> {
+    match stdio_server_bin() {
+        Ok(bin) => Ok(bin),
+        Err(_) => {
+            let status = Command::new("cargo")
+                .args([
+                    "build",
+                    "-p",
+                    "codex-rmcp-client",
+                    "--bin",
+                    "test_stdio_server",
+                ])
+                .status()
+                .context("failed to invoke cargo to build test_stdio_server")?;
+            anyhow::ensure!(
+                status.success(),
+                "cargo build -p codex-rmcp-client --bin test_stdio_server failed with status {status}"
+            );
+            stdio_server_bin()
+                .context("test_stdio_server binary still unavailable after cargo build")
+        }
+    }
+}
+
+fn create_config_toml_with_local_mcp(
+    codex_home: &Path,
+    server_uri: &str,
+    wrapper_path: &Path,
+) -> std::io::Result<()> {
+    create_config_toml(codex_home, server_uri, "never")?;
+    let config_toml = codex_home.join("config.toml");
+    let existing = std::fs::read_to_string(&config_toml)?;
+    std::fs::write(
+        &config_toml,
+        format!(
+            r#"{existing}
+
+[mcp_servers.test_stdio]
+command = "{}"
+"#,
+            wrapper_path.display(),
+        ),
+    )
+}
+
+fn create_pid_logging_stdio_wrapper(
+    dir: &Path,
+    pid_file: &Path,
+    server_bin: &str,
+) -> std::io::Result<std::path::PathBuf> {
+    let wrapper_path = dir.join("mcp-wrapper.sh");
+    std::fs::write(
+        &wrapper_path,
+        format!(
+            "#!/bin/sh\nprintf '%s\\n' \"$$\" >> '{}'\nexec '{}' \"$@\"\n",
+            pid_file.display(),
+            server_bin,
+        ),
+    )?;
+    let mut permissions = std::fs::metadata(&wrapper_path)?.permissions();
+    permissions.set_mode(0o755);
+    std::fs::set_permissions(&wrapper_path, permissions)?;
+    Ok(wrapper_path)
+}
+
+fn create_rollout(codex_home: &Path, filename_ts: &str) -> Result<String> {
+    create_fake_rollout_with_text_elements(
+        codex_home,
+        filename_ts,
+        "2025-01-05T12:00:00Z",
+        "Saved user message",
+        Vec::new(),
+        Some("mock_provider"),
+        None,
+    )
+}
+
+async fn initialize_ws_client(bind_addr: std::net::SocketAddr) -> Result<WsClient> {
+    let mut ws = connect_websocket(bind_addr).await?;
+    send_initialize_request(&mut ws, 1, "ws_disconnect_client").await?;
+    timeout(DEFAULT_READ_TIMEOUT, read_response_for_id(&mut ws, 1)).await??;
+    Ok(ws)
+}
+
+#[tokio::test]
+async fn websocket_disconnect_unloads_resumed_thread_and_reaps_stdio_mcp() -> Result<()> {
+    let server = create_mock_responses_server_repeating_assistant("Done").await;
+    let codex_home = TempDir::new()?;
+    let pid_file = codex_home.path().join("mcp-pids.log");
+    let stdio_server = ensure_stdio_server_bin()?;
+    let wrapper_path =
+        create_pid_logging_stdio_wrapper(codex_home.path(), &pid_file, &stdio_server)?;
+    create_config_toml_with_local_mcp(codex_home.path(), &server.uri(), &wrapper_path)?;
+    let conversation_id = create_rollout(codex_home.path(), "2025-01-05T12-00-00")?;
+
+    let (mut process, bind_addr) = spawn_websocket_server(codex_home.path()).await?;
+
+    let result = async {
+        let mut ws = initialize_ws_client(bind_addr).await?;
+        send_request(
+            &mut ws,
+            "thread/resume",
+            10,
+            Some(serde_json::to_value(ThreadResumeParams {
+                thread_id: conversation_id.clone(),
+                ..Default::default()
+            })?),
+        )
+        .await?;
+        let resume_resp: JSONRPCResponse =
+            timeout(DEFAULT_READ_TIMEOUT, read_response_for_id(&mut ws, 10)).await??;
+        let resume: ThreadResumeResponse = to_response::<ThreadResumeResponse>(resume_resp)?;
+        assert_eq!(resume.thread.id, conversation_id);
+
+        let pid = wait_for_pid_entry(&pid_file).await?;
+        assert!(
+            process_is_running(pid),
+            "expected stdio MCP process {pid} to be running before disconnect"
+        );
+
+        ws.close(None)
+            .await
+            .context("failed to close websocket connection")?;
+        drop(ws);
+
+        wait_for_process_exit(pid).await?;
+
+        let mut ws = connect_websocket(bind_addr).await?;
+        send_initialize_request(&mut ws, 2, "ws_disconnect_client_reconnect").await?;
+        timeout(DEFAULT_READ_TIMEOUT, read_response_for_id(&mut ws, 2)).await??;
+
+        send_request(
+            &mut ws,
+            "thread/loaded/list",
+            11,
+            Some(serde_json::to_value(ThreadLoadedListParams::default())?),
+        )
+        .await?;
+        let list_resp: JSONRPCResponse =
+            timeout(DEFAULT_READ_TIMEOUT, read_response_for_id(&mut ws, 11)).await??;
+        let ThreadLoadedListResponse { data, next_cursor } =
+            to_response::<ThreadLoadedListResponse>(list_resp)?;
+        assert_eq!(data, Vec::<String>::new());
+        assert_eq!(next_cursor, None);
+
+        Ok(())
+    }
+    .await;
+
+    process
+        .kill()
+        .await
+        .context("failed to stop websocket app-server process")?;
+    result
+}