diff --git a/codex-rs/core/src/tools/handlers/unified_exec/write_stdin.rs b/codex-rs/core/src/tools/handlers/unified_exec/write_stdin.rs
index 0b1f9d10c1..7c94948188 100644
--- a/codex-rs/core/src/tools/handlers/unified_exec/write_stdin.rs
+++ b/codex-rs/core/src/tools/handlers/unified_exec/write_stdin.rs
@@ -40,6 +40,10 @@ impl ToolExecutor<ToolInvocation> for WriteStdinHandler {
         create_write_stdin_tool()
     }
 
+    fn supports_parallel_tool_calls(&self) -> bool {
+        true
+    }
+
     fn handle(&self, invocation: ToolInvocation) -> codex_tools::ToolExecutorFuture<'_> {
         Box::pin(self.handle_call(invocation))
     }
diff --git a/codex-rs/core/src/unified_exec/process.rs b/codex-rs/core/src/unified_exec/process.rs
index 7bedfd43e3..670e94e9b6 100644
--- a/codex-rs/core/src/unified_exec/process.rs
+++ b/codex-rs/core/src/unified_exec/process.rs
@@ -82,6 +82,7 @@ pub(crate) struct UnifiedExecProcess {
     output_closed_notify: Arc<Notify>,
     cancellation_token: CancellationToken,
     output_drained: Arc<Notify>,
+    interaction_lock: Arc<Mutex<()>>,
     state_tx: watch::Sender<ProcessState>,
     state_rx: watch::Receiver<ProcessState>,
     output_task: Option<JoinHandle<()>>,
@@ -123,6 +124,7 @@ impl UnifiedExecProcess {
             output_closed_notify,
             cancellation_token,
             output_drained,
+            interaction_lock: Arc::new(Mutex::new(())),
             state_tx,
             state_rx,
             output_task: None,
@@ -178,6 +180,10 @@ impl UnifiedExecProcess {
         Arc::clone(&self.output_drained)
     }
 
+    pub(super) fn interaction_lock(&self) -> Arc<Mutex<()>> {
+        Arc::clone(&self.interaction_lock)
+    }
+
     pub(super) fn has_exited(&self) -> bool {
         let state = self.state_rx.borrow().clone();
         match &self.process_handle {
diff --git a/codex-rs/core/src/unified_exec/process_manager.rs b/codex-rs/core/src/unified_exec/process_manager.rs
index db233397b0..f828ace225 100644
--- a/codex-rs/core/src/unified_exec/process_manager.rs
+++ b/codex-rs/core/src/unified_exec/process_manager.rs
@@ -659,6 +659,19 @@ impl UnifiedExecProcessManager {
     ) -> Result<ExecCommandToolOutput, UnifiedExecError> {
         let process_id = request.process_id;
 
+        // Different terminal sessions can be polled concurrently, but reads and
+        // writes against one terminal must not overlap because they share a
+        // draining output buffer and process lifecycle.
+        let locked_process = {
+            let store = self.process_store.lock().await;
+            let entry = store
+                .processes
+                .get(&process_id)
+                .ok_or(UnifiedExecError::UnknownProcessId { process_id })?;
+            Arc::clone(&entry.process)
+        };
+        let _interaction_guard = locked_process.interaction_lock().lock_owned().await;
+
         let PreparedProcessHandles {
             process,
             output_buffer,
@@ -674,7 +687,9 @@ impl UnifiedExecProcessManager {
             process_id,
             tty,
             ..
-        } = self.prepare_process_handles(process_id).await?;
+        } = self
+            .prepare_process_handles(process_id, &locked_process)
+            .await?;
         let mut status_after_write = None;
 
         if !request.input.is_empty() {
@@ -842,12 +857,16 @@ impl UnifiedExecProcessManager {
     async fn prepare_process_handles(
         &self,
         process_id: i32,
+        expected_process: &Arc<UnifiedExecProcess>,
     ) -> Result<PreparedProcessHandles, UnifiedExecError> {
         let mut store = self.process_store.lock().await;
         let entry = store
             .processes
             .get_mut(&process_id)
             .ok_or(UnifiedExecError::UnknownProcessId { process_id })?;
+        if !Arc::ptr_eq(&entry.process, expected_process) {
+            return Err(UnifiedExecError::UnknownProcessId { process_id });
+        }
         entry.last_used = Instant::now();
         let OutputHandles {
             output_buffer,
@@ -1355,14 +1374,23 @@ impl UnifiedExecProcessManager {
             return None;
         }
 
-        let meta: Vec<(i32, Instant, bool)> = store
+        let mut meta: Vec<(i32, Instant, bool)> = store
             .processes
             .iter()
             .map(|(id, entry)| (*id, entry.last_used, entry.process.has_exited()))
             .collect();
 
-        if let Some(process_id) = Self::process_id_to_prune_from_meta(&meta) {
-            return store.remove(process_id);
+        while let Some(process_id) = Self::process_id_to_prune_from_meta(&meta) {
+            // Do not prune processes being held by write_stdin.
+            if let Some(interaction_lock) = store
+                .processes
+                .get(&process_id)
+                .map(|entry| entry.process.interaction_lock())
+                && let Ok(_interaction_guard) = interaction_lock.try_lock_owned()
+            {
+                return store.remove(process_id);
+            }
+            meta.retain(|(id, _, _)| *id != process_id);
         }
 
         None
diff --git a/codex-rs/core/tests/suite/code_mode.rs b/codex-rs/core/tests/suite/code_mode.rs
index 6edc44e297..a20eaa267a 100644
--- a/codex-rs/core/tests/suite/code_mode.rs
+++ b/codex-rs/core/tests/suite/code_mode.rs
@@ -1109,6 +1109,46 @@ text(JSON.stringify(results));
     Ok(())
 }
 
+#[cfg_attr(windows, ignore = "no exec_command on Windows")]
+#[tokio::test(flavor = "multi_thread", worker_threads = 2)]
+async fn code_mode_write_stdin_calls_run_in_parallel_across_sessions() -> Result<()> {
+    skip_if_no_network!(Ok(()));
+
+    let server = responses::start_mock_server().await;
+    let (_test, second_mock) = run_code_mode_turn(
+        &server,
+        "write to independent terminal sessions in parallel",
+        r#"
+const sessions = await Promise.all([
+  tools.exec_command({ cmd: "bash --noprofile --norc", tty: true, yield_time_ms: 250 }),
+  tools.exec_command({ cmd: "bash --noprofile --norc", tty: true, yield_time_ms: 250 }),
+]);
+
+const results = await Promise.all([
+  tools.write_stdin({
+    session_id: sessions[0].session_id,
+    chars: ": > .code-mode-a; while [ ! -e .code-mode-b ]; do sleep 0.01; done; printf 'code-alpha-%s\\n' ready; exit\n",
+    yield_time_ms: 5000,
+  }),
+  tools.write_stdin({
+    session_id: sessions[1].session_id,
+    chars: ": > .code-mode-b; while [ ! -e .code-mode-a ]; do sleep 0.01; done; printf 'code-beta-%s\\n' ready; exit\n",
+    yield_time_ms: 5000,
+  }),
+]);
+
+text(JSON.stringify([results[0].output.includes("code-alpha-ready"), results[1].output.includes("code-beta-ready")]));
+"#,
+    )
+    .await?;
+
+    let items = custom_tool_output_items(&second_mock.single_request(), "call-1");
+    let result: Value = serde_json::from_str(text_item(&items, /*index*/ 1))?;
+    assert_eq!(result, serde_json::json!([true, true]));
+
+    Ok(())
+}
+
 // This model uses token-based tool-output truncation, giving the downstream
 // history assertions a stable `…N tokens truncated…` marker.
 const TOKEN_POLICY_TEST_MODEL: &str = "gpt-5.4";
diff --git a/codex-rs/core/tests/suite/unified_exec.rs b/codex-rs/core/tests/suite/unified_exec.rs
index 46b361b73e..62b10cf424 100644
--- a/codex-rs/core/tests/suite/unified_exec.rs
+++ b/codex-rs/core/tests/suite/unified_exec.rs
@@ -3412,6 +3412,78 @@ async fn unified_exec_runs_on_all_platforms() -> Result<()> {
     Ok(())
 }
 
+#[tokio::test(flavor = "multi_thread", worker_threads = 2)]
+async fn write_stdin_calls_run_in_parallel_across_sessions() -> Result<()> {
+    skip_if_no_network!(Ok(()));
+    skip_if_target_windows!(Ok(()), "uses bash and POSIX file rendezvous commands");
+
+    let server = start_mock_server().await;
+    let mut builder = test_codex().with_model("gpt-5.4").with_config(|config| {
+        config.use_experimental_unified_exec_tool = true;
+        config
+            .features
+            .enable(Feature::UnifiedExec)
+            .expect("test config should allow feature update");
+    });
+    let test = builder.build_with_auto_env(&server).await?;
+
+    let start_args = serde_json::to_string(&json!({
+        "cmd": "bash --noprofile --norc",
+        "tty": true,
+        "yield_time_ms": 250,
+    }))?;
+    let cross_session_a = serde_json::to_string(&json!({
+        "session_id": 1000,
+        "chars": ": > .write-stdin-a; while [ ! -e .write-stdin-b ]; do sleep 0.01; done; printf 'alpha-%s\\n' ready; exit\n",
+        "yield_time_ms": 5_000,
+    }))?;
+    let cross_session_b = serde_json::to_string(&json!({
+        "session_id": 1001,
+        "chars": ": > .write-stdin-b; while [ ! -e .write-stdin-a ]; do sleep 0.01; done; printf 'beta-%s\\n' ready; exit\n",
+        "yield_time_ms": 5_000,
+    }))?;
+    let response_mock = mount_sse_sequence(
+        &server,
+        vec![
+            sse(vec![
+                ev_response_created("resp-start-1"),
+                ev_function_call("start-a", "exec_command", &start_args),
+                ev_function_call("start-b", "exec_command", &start_args),
+                ev_completed("resp-start-1"),
+            ]),
+            sse(vec![
+                ev_response_created("resp-cross-1"),
+                ev_function_call("cross-a", "write_stdin", &cross_session_a),
+                ev_function_call("cross-b", "write_stdin", &cross_session_b),
+                ev_completed("resp-cross-1"),
+            ]),
+            sse(vec![
+                ev_assistant_message("msg-done", "done"),
+                ev_completed("resp-done"),
+            ]),
+        ],
+    )
+    .await;
+
+    submit_unified_exec_turn(&test, "start terminals", PermissionProfile::Disabled).await?;
+    wait_for_event(&test.codex, |event| {
+        matches!(event, EventMsg::TurnComplete(_))
+    })
+    .await;
+
+    let outputs = collect_tool_outputs(
+        &response_mock
+            .requests()
+            .into_iter()
+            .map(|request| request.body_json())
+            .collect::<Vec<_>>(),
+    )?;
+    assert_regex_match(".*alpha-ready.*", &outputs["cross-a"].output);
+    assert_regex_match(".*beta-ready.*", &outputs["cross-b"].output);
+
+    Ok(())
+}
+
 #[tokio::test(flavor = "multi_thread", worker_threads = 2)]
 #[ignore]
 async fn unified_exec_prunes_exited_sessions_first() -> Result<()> {