diff --git a/packages/cli/src/external-listener.ts b/packages/cli/src/external-listener.ts
new file mode 100644
index 0000000000..72fbe8b13e
--- /dev/null
+++ b/packages/cli/src/external-listener.ts
@@ -0,0 +1,453 @@
+/**
+ * @license
+ * Copyright 2026 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[] = [];
+
+// Queue for unsolicited responses (e.g. Sisyphus auto-resume output)
+const unsolicitedResponses: string[] = [];
+
+/**
+ * Called by AppContainer when streaming transitions from non-Idle to Idle.
+ * If there's a pending A2A task, resolves it. Otherwise queues as unsolicited.
+ */
+export function notifyResponse(responseText: string): void {
+  if (!responseText) return;
+
+  const waiter = responseWaiters.shift();
+  if (!waiter) {
+    // No A2A task waiting — queue as unsolicited (Sisyphus, etc.)
+    unsolicitedResponses.push(responseText);
+    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);
+}
+
+/**
+ * Drain all unsolicited responses (from Sisyphus auto-resume, etc.).
+ */
+export function drainUnsolicitedResponses(): string[] {
+  return unsolicitedResponses.splice(0, unsolicitedResponses.length);
+}
+
+/**
+ * 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 handleResponsesPoll(
+  rpcId: string | number | null,
+  res: http.ServerResponse,
+): void {
+  const responses = drainUnsolicitedResponses();
+  sendJson(res, 200, jsonRpcSuccess(rpcId, { responses }));
+}
+
+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;
+                case 'responses/poll':
+                  handleResponsesPoll(rpcId, 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.tsx b/packages/cli/src/gemini.tsx
index 331ec0c018..067688306c 100644
--- a/packages/cli/src/gemini.tsx
+++ b/packages/cli/src/gemini.tsx
@@ -26,6 +26,7 @@ import { getStartupWarnings } from './utils/startupWarnings.js';
 import { getUserStartupWarnings } from './utils/userStartupWarnings.js';
 import { ConsolePatcher } from './ui/utils/ConsolePatcher.js';
 import { runNonInteractive } from './nonInteractiveCli.js';
+import { startExternalListener } from './external-listener.js';
 import {
   cleanupCheckpoints,
   registerCleanup,
@@ -322,6 +323,26 @@ export async function startInteractiveUI(
 
   registerCleanup(() => instance.unmount());
 
+  // Auto-start A2A HTTP listener in Forever Mode
+  if (config.getIsForeverMode()) {
+    const sisyphusMode = config.getSisyphusMode();
+    const a2aPort = sisyphusMode.a2aPort ?? 0;
+    try {
+      const listener = await startExternalListener({ port: a2aPort });
+      registerCleanup(listener.cleanup);
+      appEvents.emit(AppEvent.A2AListenerStarted, listener.port);
+      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)}`,
+      );
+    }
+  }
+
   registerCleanup(setupTtyCheck());
 }
 
diff --git a/packages/cli/src/ui/AppContainer.tsx b/packages/cli/src/ui/AppContainer.tsx
index 67f2d5dd84..40a63bf607 100644
--- a/packages/cli/src/ui/AppContainer.tsx
+++ b/packages/cli/src/ui/AppContainer.tsx
@@ -126,6 +126,7 @@ 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, 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';
@@ -1203,6 +1204,63 @@ Logging in with Google... Restarting Gemini CLI to continue.
     isMcpReady,
   });
 
+  // --- A2A listener integration ---
+  const [a2aListenerPort, setA2aListenerPort] = useState<number | null>(null);
+
+  useEffect(() => {
+    const handler = (port: number) => {
+      setA2aListenerPort(port);
+    };
+    appEvents.on(AppEvent.A2AListenerStarted, handler);
+    return () => {
+      appEvents.off(AppEvent.A2AListenerStarted, handler);
+    };
+  }, []);
+
+  // 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 (for A2A tasks or unsolicited output)
+    if (
+      prev !== StreamingState.Idle &&
+      streamingState === StreamingState.Idle
+    ) {
+      const history = historyManager.history;
+      const parts: string[] = [];
+      for (let i = history.length - 1; i >= 0; i--) {
+        const item = history[i];
+        if (item.type !== 'gemini' && item.type !== 'gemini_content') break;
+        if (typeof item.text === 'string' && item.text) {
+          parts.unshift(item.text);
+        }
+      }
+      notifyResponse(parts.join('\n'));
+    }
+  }, [streamingState, historyManager.history]);
+
   cancelHandlerRef.current = useCallback(
     (shouldRestorePrompt: boolean = true) => {
       const pendingHistoryItems = [
@@ -2265,6 +2323,7 @@ Logging in with Google... Restarting Gemini CLI to continue.
       adminSettingsChanged,
       newAgents,
       showIsExpandableHint,
+      a2aListenerPort,
       hintMode:
         config.isModelSteeringEnabled() &&
         isToolExecuting([
@@ -2393,6 +2452,7 @@ Logging in with Google... Restarting Gemini CLI to continue.
       adminSettingsChanged,
       newAgents,
       showIsExpandableHint,
+      a2aListenerPort,
     ],
   );
 
diff --git a/packages/cli/src/ui/components/Composer.test.tsx b/packages/cli/src/ui/components/Composer.test.tsx
index b1f804dd42..4eaa899d51 100644
--- a/packages/cli/src/ui/components/Composer.test.tsx
+++ b/packages/cli/src/ui/components/Composer.test.tsx
@@ -202,6 +202,7 @@ const createMockUIState = (overrides: Partial<UIState> = {}): UIState =>
     activeHooks: [],
     isBackgroundShellVisible: false,
     embeddedShellFocused: false,
+    a2aListenerPort: null,
     quota: {
       userTier: undefined,
       stats: undefined,
diff --git a/packages/cli/src/ui/components/StatusDisplay.test.tsx b/packages/cli/src/ui/components/StatusDisplay.test.tsx
index fcb66ea0b2..2a063df688 100644
--- a/packages/cli/src/ui/components/StatusDisplay.test.tsx
+++ b/packages/cli/src/ui/components/StatusDisplay.test.tsx
@@ -52,6 +52,7 @@ const createMockUIState = (overrides: UIStateOverrides = {}): UIState =>
     geminiMdFileCount: 0,
     contextFileNames: [],
     backgroundShellCount: 0,
+    a2aListenerPort: null,
     buffer: { text: '' },
     history: [{ id: 1, type: 'user', text: 'test' }],
     ...overrides,
@@ -171,4 +172,16 @@ describe('StatusDisplay', () => {
     expect(lastFrame()).toContain('Shells: 3');
     unmount();
   });
+
+  it('renders A2A listener port when a2aListenerPort is set', async () => {
+    const uiState = createMockUIState({
+      a2aListenerPort: 8080,
+    });
+    const { lastFrame, unmount } = await renderStatusDisplay(
+      { hideContextSummary: false },
+      uiState,
+    );
+    expect(lastFrame()).toContain('A2A :8080');
+    unmount();
+  });
 });
diff --git a/packages/cli/src/ui/components/StatusDisplay.tsx b/packages/cli/src/ui/components/StatusDisplay.tsx
index 223340c039..7a0baa524a 100644
--- a/packages/cli/src/ui/components/StatusDisplay.tsx
+++ b/packages/cli/src/ui/components/StatusDisplay.tsx
@@ -28,6 +28,12 @@ export const StatusDisplay: React.FC<StatusDisplayProps> = ({
     return <Text color={theme.status.error}>|⌐■_■|</Text>;
   }
 
+  if (uiState.a2aListenerPort !== null) {
+    return (
+      <Text color={theme.text.accent}>⚡ A2A :{uiState.a2aListenerPort}</Text>
+    );
+  }
+
   if (
     uiState.activeHooks.length > 0 &&
     settings.merged.hooksConfig.notifications
diff --git a/packages/cli/src/ui/contexts/UIStateContext.tsx b/packages/cli/src/ui/contexts/UIStateContext.tsx
index ea9025aa6b..9b9e138aae 100644
--- a/packages/cli/src/ui/contexts/UIStateContext.tsx
+++ b/packages/cli/src/ui/contexts/UIStateContext.tsx
@@ -223,6 +223,7 @@ export interface UIState {
   showIsExpandableHint: boolean;
   hintMode: boolean;
   hintBuffer: string;
+  a2aListenerPort: number | null;
   transientMessage: {
     text: string;
     type: TransientMessageType;
diff --git a/packages/cli/src/utils/events.ts b/packages/cli/src/utils/events.ts
index 8291528ac1..42340ee5c1 100644
--- a/packages/cli/src/utils/events.ts
+++ b/packages/cli/src/utils/events.ts
@@ -23,6 +23,8 @@ export enum AppEvent {
   PasteTimeout = 'paste-timeout',
   TerminalBackground = 'terminal-background',
   TransientMessage = 'transient-message',
+  ExternalMessage = 'external-message',
+  A2AListenerStarted = 'a2a-listener-started',
 }
 
 export interface AppEvents {
@@ -32,6 +34,8 @@ export interface AppEvents {
   [AppEvent.PasteTimeout]: never[];
   [AppEvent.TerminalBackground]: [string];
   [AppEvent.TransientMessage]: [TransientMessagePayload];
+  [AppEvent.ExternalMessage]: [string];
+  [AppEvent.A2AListenerStarted]: [number];
 }
 
 export const appEvents = new EventEmitter<AppEvents>();