diff --git a/packages/effect-codex-app-server/src/protocol.test.ts b/packages/effect-codex-app-server/src/protocol.test.ts
index 10e979c650108..f470d0b25bfae 100644
--- a/packages/effect-codex-app-server/src/protocol.test.ts
+++ b/packages/effect-codex-app-server/src/protocol.test.ts
@@ -5,6 +5,7 @@ import * as Queue from "effect/Queue";
 import * as Schema from "effect/Schema";
 import * as Stdio from "effect/Stdio";
 import * as Stream from "effect/Stream";
+import * as TestClock from "effect/testing/TestClock";
 
 import * as NodeServices from "@effect/platform-node/NodeServices";
 import { assert, it } from "@effect/vitest";
@@ -644,4 +645,49 @@ it.layer(NodeServices.layer)("effect-codex-app-server protocol", (it) => {
       assert.notInclude(error.message, secret);
     }),
   );
+
+  it.effect("fails pending requests when input ends while the process is still running", () =>
+    Effect.gen(function* () {
+      const { stdio, input, output } = yield* makeInMemoryStdio();
+      const transport = yield* CodexProtocol.makeCodexAppServerPatchedProtocol({
+        stdio,
+        terminationError: Effect.never,
+      });
+      const pending = yield* transport.request("thread/read", {}).pipe(Effect.forkScoped);
+      yield* Queue.take(output);
+
+      yield* Queue.end(input);
+      yield* TestClock.adjust("249 millis");
+      assert.isUndefined(pending.pollUnsafe());
+      yield* TestClock.adjust("1 millis");
+
+      const failure = yield* Fiber.join(pending).pipe(
+        Effect.match({
+          onFailure: (error) => error,
+          onSuccess: () => assert.fail("Expected the pending request to fail"),
+        }),
+      );
+      assert.instanceOf(failure, CodexError.CodexAppServerInputStreamEndedError);
+    }),
+  );
+
+  it.effect("reports a process exit that follows input end", () =>
+    Effect.gen(function* () {
+      const { stdio, input } = yield* makeInMemoryStdio();
+      const exitError = new CodexError.CodexAppServerProcessExitedError({ code: 1, pid: 123 });
+      const exited = yield* Deferred.make<CodexError.CodexAppServerError>();
+      const termination = yield* Deferred.make<CodexError.CodexAppServerError>();
+      yield* CodexProtocol.makeCodexAppServerPatchedProtocol({
+        stdio,
+        terminationError: Deferred.await(exited),
+        onTermination: (error) => Deferred.succeed(termination, error).pipe(Effect.asVoid),
+      });
+
+      yield* Queue.end(input);
+      yield* TestClock.adjust("100 millis");
+      yield* Deferred.succeed(exited, exitError);
+
+      assert.strictEqual(yield* Deferred.await(termination), exitError);
+    }),
+  );
 });
diff --git a/packages/effect-codex-app-server/src/protocol.ts b/packages/effect-codex-app-server/src/protocol.ts
index bf67174033f4d..b0ff5436e9e77 100644
--- a/packages/effect-codex-app-server/src/protocol.ts
+++ b/packages/effect-codex-app-server/src/protocol.ts
@@ -18,6 +18,7 @@ const isCodexAppServerError = Schema.is(CodexError.CodexAppServerError);
 const MAX_BUFFERED_RAW_MESSAGES = 32;
 // Bound JSONL lines before joining and parsing; the LF delimiter is excluded.
 const MAX_INCOMING_MESSAGE_BYTES = 128 * 1024 * 1024;
+const EXIT_STATUS_GRACE = "250 millis";
 
 export interface CodexAppServerProtocolLogEvent {
   readonly direction: "incoming" | "outgoing";
@@ -445,11 +446,20 @@ export const makeCodexAppServerPatchedProtocol = Effect.fn("makeCodexAppServerPa
             Effect.matchEffect({
               onFailure: (error) => handleTermination(() => Effect.succeed(error)),
               onSuccess: () =>
-                handleTermination(
-                  () =>
-                    options.terminationError ??
-                    Effect.succeed(new CodexError.CodexAppServerInputStreamEndedError({})),
-                ),
+                handleTermination(() => {
+                  const ended = new CodexError.CodexAppServerInputStreamEndedError({});
+                  // Node ends stdout before it reports the exit of a crashed process, so
+                  // wait briefly for the exit status. stdout can also close while the
+                  // process keeps running, so the wait must not hang pending requests.
+                  return options.terminationError === undefined
+                    ? Effect.succeed(ended)
+                    : options.terminationError.pipe(
+                        Effect.timeoutOrElse({
+                          duration: EXIT_STATUS_GRACE,
+                          orElse: () => Effect.succeed(ended),
+                        }),
+                      );
+                }),
             }),
           ),
       }),