diff --git a/packages/cli/src/config/config.test.ts b/packages/cli/src/config/config.test.ts
index 6e1132f5ae..0f24165df4 100644
--- a/packages/cli/src/config/config.test.ts
+++ b/packages/cli/src/config/config.test.ts
@@ -668,11 +668,20 @@ describe('parseArguments', () => {
     expect(argv.isCommand).toBe(true);
   });
 
-  it('should correctly parse the --forever flag', async () => {
+  it('should correctly parse the --forever flag and set default a2aPort to 0', async () => {
     process.argv = ['node', 'script.js', '--forever'];
     const settings = createTestMergedSettings({});
     const argv = await parseArguments(settings);
     expect(argv.forever).toBe(true);
+    expect(argv.a2aPort).toBe(0);
+  });
+
+  it('should not override explicit a2aPort when --forever is specified', async () => {
+    process.argv = ['node', 'script.js', '--forever', '--a2a-port', '8080'];
+    const settings = createTestMergedSettings({});
+    const argv = await parseArguments(settings);
+    expect(argv.forever).toBe(true);
+    expect(argv.a2aPort).toBe(8080);
   });
 });
 
diff --git a/packages/cli/src/config/config.ts b/packages/cli/src/config/config.ts
index fe5034b415..44dd66cbe0 100755
--- a/packages/cli/src/config/config.ts
+++ b/packages/cli/src/config/config.ts
@@ -103,6 +103,7 @@ export interface CliArgs {
   rawOutput: boolean | undefined;
   acceptRawOutputRisk: boolean | undefined;
   isCommand: boolean | undefined;
+  a2aPort: number | undefined;
 }
 
 export async function parseArguments(
@@ -299,6 +300,12 @@ export async function parseArguments(
         .option('accept-raw-output-risk', {
           type: 'boolean',
           description: 'Suppress the security warning when using --raw-output.',
+        })
+        .option('a2a-port', {
+          type: 'number',
+          nargs: 1,
+          description:
+            'Enable the embedded A2A HTTP listener on the specified port (0 for random). Implies --a2a enabled.',
         }),
     )
     // Register MCP subcommands
@@ -400,8 +407,15 @@ export async function parseArguments(
   (result as Record<string, unknown>)['query'] = q || undefined;
   (result as Record<string, unknown>)['startupMessages'] = startupMessages;
 
-  // The import format is now only controlled by settings.memoryImportFormat
-  // We no longer accept it as a CLI argument
+  // Enable A2A listener by default in Forever Mode
+  if (
+    result['forever'] &&
+    result['a2aPort'] === undefined &&
+    result['a2a-port'] === undefined
+  ) {
+    (result as Record<string, unknown>)['a2aPort'] = 0;
+  }
+  // The import format is now only controlled by settings.memoryImportFormat  // We no longer accept it as a CLI argument
   // eslint-disable-next-line @typescript-eslint/no-unsafe-type-assertion
   return result as unknown as CliArgs;
 }
diff --git a/packages/cli/src/external-listener.ts b/packages/cli/src/external-listener.ts
new file mode 100644
index 0000000000..5262d78970
--- /dev/null
+++ b/packages/cli/src/external-listener.ts
@@ -0,0 +1,426 @@
+/**
+ * @license
+ * Copyright 2025 Google LLC
+ * SPDX-License-Identifier: Apache-2.0
+ */
+
+import http from 'node:http';
+import { writeFileSync, mkdirSync, unlinkSync } from 'node:fs';
+import { join } from 'node:path';
+import os from 'node:os';
+import crypto from 'node:crypto';
+import { appEvents, AppEvent } from './utils/events.js';
+
+// --- A2A Task management ---
+
+interface A2AResponseMessage {
+  kind: 'message';
+  role: 'agent';
+  parts: Array<{ kind: 'text'; text: string }>;
+  messageId: string;
+}
+
+interface A2ATask {
+  id: string;
+  contextId: string;
+  status: {
+    state: 'submitted' | 'working' | 'completed' | 'failed';
+    timestamp: string;
+    message?: A2AResponseMessage;
+  };
+}
+
+const tasks = new Map<string, A2ATask>();
+
+const TASK_CLEANUP_DELAY_MS = 10 * 60 * 1000; // 10 minutes
+const DEFAULT_BLOCKING_TIMEOUT_MS = 5 * 60 * 1000; // 5 minutes
+
+interface ResponseWaiter {
+  taskId: string;
+  resolve: (text: string) => void;
+}
+
+const responseWaiters: ResponseWaiter[] = [];
+
+/**
+ * Called by AppContainer when streaming transitions from non-Idle to Idle.
+ * Resolves the oldest blocking waiter (FIFO) and completes its task.
+ */
+export function notifyResponse(responseText: string): void {
+  const waiter = responseWaiters.shift();
+  if (!waiter) return;
+
+  const task = tasks.get(waiter.taskId);
+  if (task) {
+    task.status = {
+      state: 'completed',
+      timestamp: new Date().toISOString(),
+      message: {
+        kind: 'message',
+        role: 'agent',
+        parts: [{ kind: 'text', text: responseText }],
+        messageId: crypto.randomUUID(),
+      },
+    };
+    scheduleTaskCleanup(task.id);
+  }
+
+  waiter.resolve(responseText);
+}
+
+/**
+ * Returns true if there are any in-flight tasks waiting for a response.
+ */
+export function hasPendingTasks(): boolean {
+  return responseWaiters.length > 0;
+}
+
+/**
+ * Called when streaming starts (Idle -> non-Idle) to mark the oldest
+ * submitted task as "working".
+ */
+export function markTasksWorking(): void {
+  const waiter = responseWaiters[0];
+  if (!waiter) return;
+  const task = tasks.get(waiter.taskId);
+  if (task && task.status.state === 'submitted') {
+    task.status = {
+      state: 'working',
+      timestamp: new Date().toISOString(),
+    };
+  }
+}
+
+function scheduleTaskCleanup(taskId: string): void {
+  setTimeout(() => {
+    tasks.delete(taskId);
+  }, TASK_CLEANUP_DELAY_MS);
+}
+
+function createTask(): A2ATask {
+  const task: A2ATask = {
+    id: crypto.randomUUID(),
+    contextId: `session-${process.pid}`,
+    status: {
+      state: 'submitted',
+      timestamp: new Date().toISOString(),
+    },
+  };
+  tasks.set(task.id, task);
+  return task;
+}
+
+function formatTaskResult(task: A2ATask): object {
+  return {
+    kind: 'task',
+    id: task.id,
+    contextId: task.contextId,
+    status: task.status,
+  };
+}
+
+// --- JSON-RPC helpers ---
+
+interface JsonRpcRequest {
+  jsonrpc?: string;
+  id?: string | number | null;
+  method?: string;
+  params?: Record<string, unknown>;
+}
+
+function jsonRpcSuccess(id: string | number | null, result: object): object {
+  return { jsonrpc: '2.0', id, result };
+}
+
+function jsonRpcError(
+  id: string | number | null,
+  code: number,
+  message: string,
+): object {
+  return { jsonrpc: '2.0', id, error: { code, message } };
+}
+
+// --- HTTP utilities ---
+
+function getSessionsDir(): string {
+  return join(os.homedir(), '.gemini', 'sessions');
+}
+
+function getPortFilePath(): string {
+  return join(getSessionsDir(), `interactive-${process.pid}.port`);
+}
+
+function buildAgentCard(port: number): object {
+  return {
+    name: 'Gemini CLI Interactive Session',
+    url: `http://localhost:${port}/`,
+    protocolVersion: '0.3.0',
+    provider: { organization: 'Google', url: 'https://google.com' },
+    capabilities: { streaming: false, pushNotifications: false },
+    defaultInputModes: ['text'],
+    defaultOutputModes: ['text'],
+    skills: [
+      {
+        id: 'interactive_session',
+        name: 'Interactive Session',
+        description: 'Send messages to the live interactive Gemini CLI session',
+      },
+    ],
+  };
+}
+
+interface A2AMessagePart {
+  kind?: string;
+  text?: string;
+}
+
+function extractTextFromParts(
+  parts: A2AMessagePart[] | undefined,
+): string | null {
+  if (!Array.isArray(parts)) {
+    return null;
+  }
+  const texts: string[] = [];
+  for (const part of parts) {
+    if (part.kind === 'text' && typeof part.text === 'string') {
+      texts.push(part.text);
+    }
+  }
+  return texts.length > 0 ? texts.join('\n') : null;
+}
+
+function sendJson(
+  res: http.ServerResponse,
+  statusCode: number,
+  data: object,
+): void {
+  const body = JSON.stringify(data);
+  res.writeHead(statusCode, {
+    'Content-Type': 'application/json',
+    'Content-Length': Buffer.byteLength(body),
+  });
+  res.end(body);
+}
+
+function readBody(req: http.IncomingMessage): Promise<string> {
+  return new Promise((resolve, reject) => {
+    const chunks: Buffer[] = [];
+    let size = 0;
+    const maxSize = 1024 * 1024; // 1MB limit
+    req.on('data', (chunk: Buffer) => {
+      size += chunk.length;
+      if (size > maxSize) {
+        req.destroy();
+        reject(new Error('Request body too large'));
+        return;
+      }
+      chunks.push(chunk);
+    });
+    req.on('end', () => resolve(Buffer.concat(chunks).toString('utf-8')));
+    req.on('error', reject);
+  });
+}
+
+// --- JSON-RPC request handlers ---
+
+function handleMessageSend(
+  rpcId: string | number | null,
+  params: Record<string, unknown>,
+  res: http.ServerResponse,
+): void {
+  const messageVal = params['message'];
+  const message =
+    messageVal && typeof messageVal === 'object'
+      ? (messageVal as { role?: string; parts?: A2AMessagePart[] })
+      : undefined;
+  const text = extractTextFromParts(message?.parts);
+  if (!text) {
+    sendJson(
+      res,
+      200,
+      jsonRpcError(
+        rpcId,
+        -32602,
+        'Missing or empty text. Expected: params.message.parts with kind "text".',
+      ),
+    );
+    return;
+  }
+
+  const task = createTask();
+
+  // Inject message into the session
+  appEvents.emit(AppEvent.ExternalMessage, text);
+
+  // Block until response (standard A2A message/send semantics)
+  const timer = setTimeout(() => {
+    const idx = responseWaiters.findIndex((w) => w.taskId === task.id);
+    if (idx !== -1) {
+      responseWaiters.splice(idx, 1);
+    }
+    task.status = {
+      state: 'failed',
+      timestamp: new Date().toISOString(),
+    };
+    scheduleTaskCleanup(task.id);
+    sendJson(res, 200, jsonRpcError(rpcId, -32000, 'Request timed out'));
+  }, DEFAULT_BLOCKING_TIMEOUT_MS);
+
+  responseWaiters.push({
+    taskId: task.id,
+    resolve: () => {
+      clearTimeout(timer);
+      // Task is already updated in notifyResponse
+      const updatedTask = tasks.get(task.id);
+      sendJson(
+        res,
+        200,
+        jsonRpcSuccess(rpcId, formatTaskResult(updatedTask ?? task)),
+      );
+    },
+  });
+}
+
+function handleTasksGet(
+  rpcId: string | number | null,
+  params: Record<string, unknown>,
+  res: http.ServerResponse,
+): void {
+  const taskId = params['id'];
+  if (typeof taskId !== 'string') {
+    sendJson(
+      res,
+      200,
+      jsonRpcError(rpcId, -32602, 'Missing or invalid params.id'),
+    );
+    return;
+  }
+
+  const task = tasks.get(taskId);
+  if (!task) {
+    sendJson(res, 200, jsonRpcError(rpcId, -32001, 'Task not found'));
+    return;
+  }
+
+  sendJson(res, 200, jsonRpcSuccess(rpcId, formatTaskResult(task)));
+}
+
+// --- Server ---
+
+export interface ExternalListenerResult {
+  port: number;
+  cleanup: () => void;
+}
+
+/**
+ * Start an embedded HTTP server that accepts A2A-format JSON-RPC messages
+ * and bridges them into the interactive session's message queue.
+ */
+export function startExternalListener(options?: {
+  port?: number;
+}): Promise<ExternalListenerResult> {
+  const port = options?.port ?? 0;
+
+  return new Promise((resolve, reject) => {
+    const server = http.createServer(
+      (req: http.IncomingMessage, res: http.ServerResponse) => {
+        const url = new URL(req.url ?? '/', `http://localhost`);
+
+        // GET /.well-known/agent-card.json
+        if (
+          req.method === 'GET' &&
+          url.pathname === '/.well-known/agent-card.json'
+        ) {
+          const address = server.address();
+          const actualPort =
+            typeof address === 'object' && address ? address.port : port;
+          sendJson(res, 200, buildAgentCard(actualPort));
+          return;
+        }
+
+        // POST / — JSON-RPC 2.0 routing
+        if (req.method === 'POST' && url.pathname === '/') {
+          readBody(req)
+            .then((rawBody) => {
+              let parsed: JsonRpcRequest;
+              try {
+                // eslint-disable-next-line @typescript-eslint/no-unsafe-type-assertion
+                parsed = JSON.parse(rawBody) as JsonRpcRequest;
+              } catch {
+                sendJson(
+                  res,
+                  200,
+                  jsonRpcError(null, -32700, 'Parse error: invalid JSON'),
+                );
+                return;
+              }
+
+              const rpcId = parsed.id ?? null;
+              const method = parsed.method;
+              const params = parsed.params ?? {};
+
+              switch (method) {
+                case 'message/send':
+                  handleMessageSend(rpcId, params, res);
+                  break;
+                case 'tasks/get':
+                  handleTasksGet(rpcId, params, res);
+                  break;
+                default:
+                  sendJson(
+                    res,
+                    200,
+                    jsonRpcError(
+                      rpcId,
+                      -32601,
+                      `Method not found: ${method ?? '(none)'}`,
+                    ),
+                  );
+              }
+            })
+            .catch(() => {
+              sendJson(
+                res,
+                200,
+                jsonRpcError(null, -32603, 'Failed to read request body'),
+              );
+            });
+          return;
+        }
+
+        // 404 for everything else
+        sendJson(res, 404, { error: 'Not found' });
+      },
+    );
+
+    server.listen(port, '127.0.0.1', () => {
+      const address = server.address();
+      const actualPort =
+        typeof address === 'object' && address ? address.port : port;
+
+      // Write port file
+      try {
+        const sessionsDir = getSessionsDir();
+        mkdirSync(sessionsDir, { recursive: true });
+        writeFileSync(getPortFilePath(), String(actualPort), 'utf-8');
+      } catch {
+        // Non-fatal: port file is a convenience, not a requirement
+      }
+
+      const cleanup = () => {
+        server.close();
+        try {
+          unlinkSync(getPortFilePath());
+        } catch {
+          // Ignore: file may already be deleted
+        }
+      };
+
+      resolve({ port: actualPort, cleanup });
+    });
+
+    server.on('error', (err) => {
+      reject(err);
+    });
+  });
+}
diff --git a/packages/cli/src/gemini.test.tsx b/packages/cli/src/gemini.test.tsx
index 80a5b8d090..d6755aa25e 100644
--- a/packages/cli/src/gemini.test.tsx
+++ b/packages/cli/src/gemini.test.tsx
@@ -499,6 +499,7 @@ describe('gemini.tsx main function kitty protocol', () => {
       rawOutput: undefined,
       acceptRawOutputRisk: undefined,
       isCommand: undefined,
+      a2aPort: undefined,
     });
 
     await act(async () => {
diff --git a/packages/cli/src/gemini.tsx b/packages/cli/src/gemini.tsx
index aa830c0250..6f897b526f 100644
--- a/packages/cli/src/gemini.tsx
+++ b/packages/cli/src/gemini.tsx
@@ -82,6 +82,7 @@ import { validateNonInteractiveAuth } from './validateNonInterActiveAuth.js';
 import { checkForUpdates } from './ui/utils/updateCheck.js';
 import { handleAutoUpdate } from './utils/handleAutoUpdate.js';
 import { appEvents, AppEvent } from './utils/events.js';
+import { startExternalListener } from './external-listener.js';
 import { SessionSelector } from './utils/sessionUtils.js';
 import { SettingsContext } from './ui/contexts/SettingsContext.js';
 import { MouseProvider } from './ui/contexts/MouseContext.js';
@@ -188,6 +189,7 @@ export async function startInteractiveUI(
   workspaceRoot: string = process.cwd(),
   resumedSessionData: ResumedSessionData | undefined,
   initializationResult: InitializationResult,
+  a2aPort?: number,
 ) {
   // Never enter Ink alternate buffer mode when screen reader mode is enabled
   // as there is no benefit of alternate buffer mode when using a screen reader
@@ -319,6 +321,23 @@ export async function startInteractiveUI(
     });
 
   registerCleanup(() => instance.unmount());
+
+  // Start embedded A2A HTTP listener if enabled via --a2a-port
+  if (a2aPort !== undefined) {
+    try {
+      const listener = await startExternalListener({ port: a2aPort });
+      registerCleanup(listener.cleanup);
+      coreEvents.emitFeedback(
+        'info',
+        `A2A endpoint listening on port ${listener.port}`,
+      );
+    } catch (err) {
+      coreEvents.emitFeedback(
+        'warning',
+        `Failed to start A2A listener: ${err instanceof Error ? err.message : String(err)}`,
+      );
+    }
+  }
 }
 
 export async function main() {
@@ -722,6 +741,7 @@ export async function main() {
         process.cwd(),
         resumedSessionData,
         initializationResult,
+        argv.a2aPort,
       );
       return;
     }
diff --git a/packages/cli/src/ui/AppContainer.tsx b/packages/cli/src/ui/AppContainer.tsx
index 0c3a6e1d9d..e49aa62ecd 100644
--- a/packages/cli/src/ui/AppContainer.tsx
+++ b/packages/cli/src/ui/AppContainer.tsx
@@ -123,6 +123,11 @@ import { useFolderTrust } from './hooks/useFolderTrust.js';
 import { useIdeTrustListener } from './hooks/useIdeTrustListener.js';
 import { type IdeIntegrationNudgeResult } from './IdeIntegrationNudge.js';
 import { appEvents, AppEvent, TransientMessageType } from '../utils/events.js';
+import {
+  notifyResponse,
+  hasPendingTasks,
+  markTasksWorking,
+} from '../external-listener.js';
 import { type UpdateObject } from './utils/updateCheck.js';
 import { setUpdateHandler } from '../utils/handleAutoUpdate.js';
 import { registerCleanup, runExitCleanup } from '../utils/cleanup.js';
@@ -1199,6 +1204,49 @@ Logging in with Google... Restarting Gemini CLI to continue.
     isMcpReady,
   });
 
+  // Bridge external messages from A2A HTTP listener to message queue
+  useEffect(() => {
+    const handler = (text: string) => {
+      addMessage(text);
+    };
+    appEvents.on(AppEvent.ExternalMessage, handler);
+    return () => {
+      appEvents.off(AppEvent.ExternalMessage, handler);
+    };
+  }, [addMessage]);
+
+  // Track streaming state transitions for A2A response capture
+  const prevStreamingStateRef = useRef(streamingState);
+
+  useEffect(() => {
+    const prev = prevStreamingStateRef.current;
+    prevStreamingStateRef.current = streamingState;
+
+    // Mark tasks as "working" when streaming starts
+    if (
+      prev === StreamingState.Idle &&
+      streamingState !== StreamingState.Idle
+    ) {
+      markTasksWorking();
+    }
+
+    // Capture response when streaming ends
+    if (
+      prev !== StreamingState.Idle &&
+      streamingState === StreamingState.Idle &&
+      hasPendingTasks()
+    ) {
+      const lastResponse = historyManager.history
+        .slice()
+        .reverse()
+        .find((item) => item.type === 'gemini');
+      notifyResponse(
+        typeof lastResponse?.text === 'string' ? lastResponse.text : '',
+      );
+    }
+    // eslint-disable-next-line react-hooks/exhaustive-deps
+  }, [streamingState]);
+
   cancelHandlerRef.current = useCallback(
     (shouldRestorePrompt: boolean = true) => {
       const pendingHistoryItems = [
diff --git a/packages/cli/src/utils/events.ts b/packages/cli/src/utils/events.ts
index 8291528ac1..b8088da24f 100644
--- a/packages/cli/src/utils/events.ts
+++ b/packages/cli/src/utils/events.ts
@@ -23,6 +23,7 @@ export enum AppEvent {
   PasteTimeout = 'paste-timeout',
   TerminalBackground = 'terminal-background',
   TransientMessage = 'transient-message',
+  ExternalMessage = 'external-message',
 }
 
 export interface AppEvents {
@@ -32,6 +33,7 @@ export interface AppEvents {
   [AppEvent.PasteTimeout]: never[];
   [AppEvent.TerminalBackground]: [string];
   [AppEvent.TransientMessage]: [TransientMessagePayload];
+  [AppEvent.ExternalMessage]: [string];
 }
 
 export const appEvents = new EventEmitter<AppEvents>();