diff --git a/codex-rs/core/tests/suite/mod.rs b/codex-rs/core/tests/suite/mod.rs
index 3e27463370..1b0de3b264 100644
--- a/codex-rs/core/tests/suite/mod.rs
+++ b/codex-rs/core/tests/suite/mod.rs
@@ -99,6 +99,7 @@ mod request_permissions_tool;
 mod request_plugin_install;
 mod request_user_input;
 mod responses_api_proxy_headers;
+mod responses_api_system_proxy;
 mod responses_lite;
 mod resume;
 mod resume_warning;
diff --git a/codex-rs/core/tests/suite/responses_api_system_proxy.rs b/codex-rs/core/tests/suite/responses_api_system_proxy.rs
new file mode 100644
index 0000000000..0a1f998896
--- /dev/null
+++ b/codex-rs/core/tests/suite/responses_api_system_proxy.rs
@@ -0,0 +1,117 @@
+//! Verifies that the effective system-proxy feature reaches both HTTP Responses API paths.
+
+use anyhow::Result;
+use codex_config::CONFIG_TOML_FILE;
+use codex_protocol::models::ResponseItem;
+use codex_protocol::protocol::EventMsg;
+use codex_protocol::protocol::Op;
+use core_test_support::responses::ev_completed;
+use core_test_support::responses::ev_response_created;
+use core_test_support::responses::mount_compact_json_once;
+use core_test_support::responses::mount_sse_once;
+use core_test_support::responses::sse;
+use core_test_support::responses::start_mock_server;
+use core_test_support::skip_if_no_network;
+use core_test_support::test_codex::test_codex;
+use core_test_support::wait_for_event;
+use pretty_assertions::assert_eq;
+use std::process::Command;
+
+const SUBPROCESS_ENV: &str = "CODEX_RESPONSES_SYSTEM_PROXY_TEST_CHILD";
+const SUBPROCESS_SENTINEL: &str = "responses system proxy child ran";
+const TEST_NAME: &str =
+    "suite::responses_api_system_proxy::responses_and_compact_use_enabled_system_proxy";
+const TARGET_BASE_URL: &str = "http://responses-api.invalid/v1";
+
+#[cfg_attr(
+    not(target_os = "linux"),
+    ignore = "system proxy environment fallback is Linux-specific"
+)]
+#[tokio::test(flavor = "multi_thread", worker_threads = 2)]
+async fn responses_and_compact_use_enabled_system_proxy() -> Result<()> {
+    if std::env::var_os(SUBPROCESS_ENV).is_none() {
+        return run_test_in_subprocess().await;
+    }
+
+    eprintln!("{SUBPROCESS_SENTINEL}");
+    skip_if_no_network!(Ok(()));
+
+    let server = start_mock_server().await;
+    let mut builder = test_codex()
+        .with_pre_build_hook(|codex_home| {
+            std::fs::write(
+                codex_home.join(CONFIG_TOML_FILE),
+                "[features]\nrespect_system_proxy = true\n",
+            )
+            .expect("system-proxy feature config should be written");
+        })
+        .with_config(|config| {
+            config.model_provider.base_url = Some(TARGET_BASE_URL.to_string());
+        });
+    let test = builder.build_with_auto_env(&server).await?;
+    assert!(test.config.respect_system_proxy);
+
+    test.submit_turn("exercise the Responses API proxy route")
+        .await?;
+    test.codex.submit(Op::Compact).await?;
+    wait_for_event(&test.codex, |event| {
+        matches!(event, EventMsg::TurnComplete(_))
+    })
+    .await;
+
+    Ok(())
+}
+
+async fn run_test_in_subprocess() -> Result<()> {
+    skip_if_no_network!(Ok(()));
+
+    let proxy = start_mock_server().await;
+    let responses_mock = mount_sse_once(
+        &proxy,
+        sse(vec![ev_response_created("resp-1"), ev_completed("resp-1")]),
+    )
+    .await;
+    let compact_mock = mount_compact_json_once(
+        &proxy,
+        serde_json::json!({
+            "output": [ResponseItem::Compaction {
+                id: None,
+                encrypted_content: "encrypted compacted history".to_string(),
+                internal_chat_message_metadata_passthrough: None,
+            }]
+        }),
+    )
+    .await;
+
+    // Reqwest disables its default environment proxy matcher in CGI processes. The route-aware
+    // client resolves `HTTP_PROXY` explicitly, so this marker makes the test fail if either
+    // Responses endpoint regresses to the default client.
+    let output = Command::new(std::env::current_exe()?)
+        .args(["--exact", TEST_NAME, "--nocapture"])
+        .env(SUBPROCESS_ENV, "1")
+        .env("HTTP_PROXY", proxy.uri())
+        .env("REQUEST_METHOD", "GET")
+        .env_remove("http_proxy")
+        .env_remove("ALL_PROXY")
+        .env_remove("all_proxy")
+        .env_remove("NO_PROXY")
+        .env_remove("no_proxy")
+        .output()?;
+    let stderr = String::from_utf8_lossy(&output.stderr);
+    assert!(
+        output.status.success(),
+        "system-proxy subprocess failed\nstdout:\n{}\nstderr:\n{stderr}",
+        String::from_utf8_lossy(&output.stdout),
+    );
+    assert!(
+        stderr.contains(SUBPROCESS_SENTINEL),
+        "system-proxy subprocess did not execute the expected test\nstderr:\n{stderr}"
+    );
+
+    assert_eq!(responses_mock.single_request().path(), "/v1/responses");
+    assert_eq!(
+        compact_mock.single_request().path(),
+        "/v1/responses/compact"
+    );
+    Ok(())
+}