diff --git a/packages/cli/src/utils/readStdin.test.ts b/packages/cli/src/utils/readStdin.test.ts
index 5cc187fcbe..1a5202173c 100644
--- a/packages/cli/src/utils/readStdin.test.ts
+++ b/packages/cli/src/utils/readStdin.test.ts
@@ -21,6 +21,8 @@ const mockStdin = {
   on: vi.fn(),
   removeListener: vi.fn(),
   destroy: vi.fn(),
+  listeners: vi.fn().mockReturnValue([]),
+  listenerCount: vi.fn().mockReturnValue(0),
 };
 
 describe('readStdin', () => {
@@ -48,6 +50,8 @@ describe('readStdin', () => {
         if (event === 'error') onErrorHandler = handler as (err: Error) => void;
       },
     );
+    mockStdin.listeners.mockReturnValue([]);
+    mockStdin.listenerCount.mockReturnValue(0);
   });
 
   afterEach(() => {
diff --git a/packages/cli/src/utils/readStdin.ts b/packages/cli/src/utils/readStdin.ts
index cd62d1f961..30834e0d14 100644
--- a/packages/cli/src/utils/readStdin.ts
+++ b/packages/cli/src/utils/readStdin.ts
@@ -62,6 +62,13 @@ export async function readStdin(): Promise<string> {
       process.stdin.removeListener('readable', onReadable);
       process.stdin.removeListener('end', onEnd);
       process.stdin.removeListener('error', onError);
+
+      // Add a no-op error listener if no other error listeners are present to prevent
+      // unhandled 'error' events (like EIO) from crashing the process after we stop reading.
+      // This is especially important for background execution where TTY might cause EIO.
+      if (process.stdin.listenerCount('error') === 0) {
+        process.stdin.on('error', noopErrorHandler);
+      }
     };
 
     process.stdin.on('readable', onReadable);
@@ -69,3 +76,5 @@ export async function readStdin(): Promise<string> {
     process.stdin.on('error', onError);
   });
 }
+
+function noopErrorHandler() {}
diff --git a/packages/cli/src/utils/readStdin_safety.test.ts b/packages/cli/src/utils/readStdin_safety.test.ts
new file mode 100644
index 0000000000..4e4ba08f6d
--- /dev/null
+++ b/packages/cli/src/utils/readStdin_safety.test.ts
@@ -0,0 +1,92 @@
+/**
+ * @license
+ * Copyright 2025 Google LLC
+ * SPDX-License-Identifier: Apache-2.0
+ */
+
+import { vi, describe, expect, it, beforeEach, afterEach } from 'vitest';
+import { readStdin } from './readStdin.js';
+import { EventEmitter } from 'node:events';
+
+// Mock debugLogger to avoid clutter
+vi.mock('@google/gemini-cli-core', () => ({
+  debugLogger: {
+    warn: vi.fn(),
+  },
+}));
+
+describe('readStdin EIO Reproduction', () => {
+  let originalStdin: typeof process.stdin;
+  // eslint-disable-next-line @typescript-eslint/no-explicit-any
+  let fakeStdin: EventEmitter & { setEncoding: any; read: any; destroy: any };
+
+  beforeEach(() => {
+    originalStdin = process.stdin;
+    // eslint-disable-next-line @typescript-eslint/no-explicit-any
+    fakeStdin = new EventEmitter() as any;
+    fakeStdin.setEncoding = vi.fn();
+    fakeStdin.read = vi.fn().mockReturnValue(null); // Return null to simulate end of reading or no data
+    fakeStdin.destroy = vi.fn();
+
+    Object.defineProperty(process, 'stdin', {
+      value: fakeStdin,
+      writable: true,
+      configurable: true,
+    });
+  });
+
+  afterEach(() => {
+    Object.defineProperty(process, 'stdin', {
+      value: originalStdin,
+      writable: true,
+      configurable: true,
+    });
+    vi.restoreAllMocks();
+  });
+
+  it('crashes (throws unhandled error) if EIO happens after readStdin completes', async () => {
+    const promise = readStdin();
+    fakeStdin.emit('end');
+    await promise;
+
+    // Verify listeners are removed (implementation detail check)
+
+    // We expect 1 listener now (our no-op handler) because we started with 0.
+
+    expect(fakeStdin.listenerCount('error')).toBe(1);
+
+    // This mimics the crash.
+
+    // We expect this NOT to throw now that we've added a no-op handler.
+
+    expect(() => {
+      fakeStdin.emit('error', new Error('EIO'));
+    }).not.toThrow();
+  });
+
+  it('does NOT add a no-op handler if another error listener is present', async () => {
+    const customErrorHandler = vi.fn();
+
+    fakeStdin.on('error', customErrorHandler);
+
+    const promise = readStdin();
+
+    fakeStdin.emit('end');
+
+    await promise;
+
+    // It should have exactly 1 listener (our custom one), not 2.
+
+    expect(fakeStdin.listenerCount('error')).toBe(1);
+
+    expect(fakeStdin.listeners('error')).toContain(customErrorHandler);
+
+    // Triggering error should call our handler and NOT crash (because there is a listener)
+
+    const error = new Error('EIO');
+
+    fakeStdin.emit('error', error);
+
+    expect(customErrorHandler).toHaveBeenCalledWith(error);
+  });
+});