diff --git a/src/cli/operations/dev/web-ui/__tests__/local-agui-invocations.test.ts b/src/cli/operations/dev/web-ui/__tests__/local-agui-invocations.test.ts
new file mode 100644
index 000000000..33fe6a52e
--- /dev/null
+++ b/src/cli/operations/dev/web-ui/__tests__/local-agui-invocations.test.ts
@@ -0,0 +1,110 @@
+import { handleInvocations } from '../handlers/invocations.js';
+import type { RouteContext } from '../handlers/route-context.js';
+import { EventEmitter } from 'node:events';
+import type { IncomingMessage, ServerResponse } from 'node:http';
+import { beforeEach, describe, expect, it, vi } from 'vitest';
+
+const { capturedBodies, requestMock } = vi.hoisted(() => ({
+  capturedBodies: [] as string[],
+  requestMock: vi.fn(),
+}));
+
+vi.mock('node:http', () => ({
+  request: requestMock,
+}));
+
+interface MockRes extends ServerResponse {
+  _status: number;
+  _headers: Record<string, string>;
+  _chunks: string[];
+}
+
+function mockRes(): MockRes {
+  const res = {
+    _status: 0,
+    _headers: {} as Record<string, string>,
+    _chunks: [] as string[],
+    headersSent: false,
+    writeHead(status: number, headers?: Record<string, string>) {
+      res._status = status;
+      res.headersSent = true;
+      if (headers) Object.assign(res._headers, headers);
+      return res;
+    },
+    setHeader(name: string, value: string) {
+      res._headers[name] = value;
+    },
+    write(chunk: string) {
+      res._chunks.push(chunk);
+      return true;
+    },
+    end(body?: string) {
+      if (body) res._chunks.push(body);
+      return res;
+    },
+  };
+  return res as unknown as MockRes;
+}
+
+function mockReq(): IncomingMessage {
+  return { url: '/invocations', headers: { host: 'localhost:8081' } } as unknown as IncomingMessage;
+}
+
+function mockCtx(bodyValue: string): RouteContext {
+  return {
+    options: {
+      mode: 'dev',
+      agents: [],
+      harnesses: [],
+      uiPort: 8081,
+      configRoot: '/tmp/test-project/agentcore',
+    },
+    runningAgents: new Map([['agui-agent', { server: {} as never, port: 8082, protocol: 'AGUI' }]]),
+    startingAgents: new Map(),
+    agentErrors: new Map(),
+    setCorsHeaders: vi.fn(),
+    readBody: vi.fn().mockResolvedValue(bodyValue),
+  } as RouteContext;
+}
+
+describe('handleInvocations local AGUI proxy', () => {
+  beforeEach(() => {
+    capturedBodies.length = 0;
+    requestMock.mockReset();
+    requestMock.mockImplementation((_options, callback: (res: EventEmitter & Record<string, unknown>) => void) => {
+      const proxyReq = new EventEmitter() as EventEmitter & {
+        end: ReturnType<typeof vi.fn>;
+        write: ReturnType<typeof vi.fn>;
+      };
+      proxyReq.write = vi.fn((chunk: string) => {
+        capturedBodies.push(chunk);
+        return true;
+      });
+      proxyReq.end = vi.fn(() => {
+        const agentRes = new EventEmitter() as EventEmitter & Record<string, unknown>;
+        agentRes.headers = { 'content-type': 'text/event-stream' };
+        agentRes.statusCode = 200;
+        agentRes.pipe = vi.fn((res: MockRes) => {
+          res.write('data: {"type":"RUN_FINISHED"}\n\n');
+          return res;
+        });
+        callback(agentRes);
+        agentRes.emit('end');
+      });
+      return proxyReq;
+    });
+  });
+
+  it('uses the browser session id as the AGUI thread id across messages', async () => {
+    const firstBody = JSON.stringify({ agentName: 'agui-agent', prompt: 'hello', sessionId: 'browser-session-1' });
+    const secondBody = JSON.stringify({ agentName: 'agui-agent', prompt: 'again', sessionId: 'browser-session-1' });
+
+    await handleInvocations(mockCtx(firstBody), mockReq(), mockRes());
+    await handleInvocations(mockCtx(secondBody), mockReq(), mockRes());
+
+    const aguiBodies = capturedBodies.map(body => JSON.parse(body) as { threadId: string; runId: string });
+    expect(aguiBodies).toHaveLength(2);
+    expect(aguiBodies.map(body => body.threadId)).toEqual(['browser-session-1', 'browser-session-1']);
+    expect(aguiBodies[0]!.runId).not.toBe(aguiBodies[1]!.runId);
+  });
+});
diff --git a/src/cli/operations/dev/web-ui/handlers/invocations.ts b/src/cli/operations/dev/web-ui/handlers/invocations.ts
index 906eecd3c..fa55f9110 100644
--- a/src/cli/operations/dev/web-ui/handlers/invocations.ts
+++ b/src/cli/operations/dev/web-ui/handlers/invocations.ts
@@ -300,15 +300,7 @@ async function handleAguiInvocation(
   }
 
   // Build RunAgentInput — the body format AGUI agents expect
-  const aguiBody = JSON.stringify({
-    threadId: randomUUID(),
-    runId: randomUUID(),
-    messages: [{ id: randomUUID(), role: 'user', content: prompt }],
-    tools: [],
-    context: [],
-    state: {},
-    forwardedProps: {},
-  });
+  const aguiBody = JSON.stringify(buildAguiRunInput(prompt, sessionId));
 
   // Proxy to agent, piping the SSE response through untouched
   return new Promise<void>((resolve, reject) => {