diff --git a/packages/runtime/src/handlers/websocket.ts b/packages/runtime/src/handlers/websocket.ts
index 014dfc44b..d4b556bb7 100644
--- a/packages/runtime/src/handlers/websocket.ts
+++ b/packages/runtime/src/handlers/websocket.ts
@@ -2,6 +2,7 @@ import type { Context, MiddlewareHandler } from 'hono';
 import { upgradeWebSocket } from 'hono/bun';
 import { context as otelContext, ROOT_CONTEXT } from '@opentelemetry/api';
 import type { Env } from '../app';
+import { getAgentAsyncLocalStorage, getHTTPAsyncLocalStorage } from '../_context';
 import { tagRoute } from './_route-meta';
 
 /**
@@ -100,6 +101,10 @@ export function websocket<E extends Env = Env>(
 		let messageHandler: ((event: MessageEvent) => void | Promise<void>) | undefined;
 		let closeHandler: ((event: CloseEvent) => void | Promise<void>) | undefined;
 		let initialized = false;
+		const agentAsyncLocalStorage = getAgentAsyncLocalStorage();
+		const httpAsyncLocalStorage = getHTTPAsyncLocalStorage();
+		const capturedAgentContext = agentAsyncLocalStorage.getStore();
+		const capturedHTTPContext = httpAsyncLocalStorage.getStore();
 
 		// Create done promise for session lifecycle deferral, but ONLY for actual
 		// WebSocket upgrade requests. The factory runs unconditionally for every
@@ -137,12 +142,29 @@ export function websocket<E extends Env = Env>(
 			},
 		};
 
+		const runWithCapturedContext = <T>(callback: () => T): T => {
+			return otelContext.with(ROOT_CONTEXT, () => {
+				const runWithAgentContext = () => {
+					if (capturedAgentContext) {
+						return agentAsyncLocalStorage.run(capturedAgentContext, callback);
+					}
+					return callback();
+				};
+
+				if (capturedHTTPContext) {
+					return httpAsyncLocalStorage.run(capturedHTTPContext, runWithAgentContext);
+				}
+
+				return runWithAgentContext();
+			});
+		};
+
 		// IMPORTANT: We run in ROOT_CONTEXT (no active OTEL span) to avoid a Bun bug
 		// where OTEL-instrumented fetch conflicts with streaming responses.
 		// See: https://github.com/agentuity/sdk/issues/471
 		// See: https://github.com/oven-sh/bun/issues/24766
 		const runHandler = () => {
-			otelContext.with(ROOT_CONTEXT, () => {
+			runWithCapturedContext(() => {
 				handler(c, wsConnection);
 			});
 			initialized = true;
@@ -157,7 +179,7 @@ export function websocket<E extends Env = Env>(
 					wsConnection.send = (data) => ws.send(data);
 
 					if (openHandler) {
-						await otelContext.with(ROOT_CONTEXT, () => openHandler!(event));
+						await runWithCapturedContext(() => openHandler!(event));
 					}
 				} catch (err) {
 					c.var.logger?.error('WebSocket onOpen error:', err);
@@ -172,7 +194,7 @@ export function websocket<E extends Env = Env>(
 						runHandler();
 					}
 					if (messageHandler) {
-						await otelContext.with(ROOT_CONTEXT, () => messageHandler!(event));
+						await runWithCapturedContext(() => messageHandler!(event));
 					}
 				} catch (err) {
 					c.var.logger?.error('WebSocket onMessage error:', err);
@@ -183,7 +205,7 @@ export function websocket<E extends Env = Env>(
 			onClose: async (event: CloseEvent, _ws: any) => {
 				try {
 					if (closeHandler) {
-						await otelContext.with(ROOT_CONTEXT, () => closeHandler!(event));
+						await runWithCapturedContext(() => closeHandler!(event));
 					}
 				} catch (err) {
 					c.var.logger?.error('WebSocket onClose error:', err);
diff --git a/packages/runtime/test/websocket-agent-context.test.ts b/packages/runtime/test/websocket-agent-context.test.ts
new file mode 100644
index 000000000..d03e9c936
--- /dev/null
+++ b/packages/runtime/test/websocket-agent-context.test.ts
@@ -0,0 +1,277 @@
+import { describe, expect, test } from 'bun:test';
+import type { AuthInterface } from '@agentuity/auth/types';
+import { trace } from '@opentelemetry/api';
+import { Hono } from 'hono';
+import { websocket as bunWebsocket } from 'hono/bun';
+import { runInHTTPContext } from '../src/_context';
+import { createAgent, createAgentMiddleware } from '../src/agent';
+import { websocket } from '../src/handlers/websocket';
+import type { Logger } from '../src/logger';
+import type { Session, Thread } from '../src/session';
+import WaitUntilHandler from '../src/_waituntil';
+import { z } from 'zod';
+
+interface EchoReadyMessage {
+	type: 'ready';
+}
+
+interface EchoSuccessMessage {
+	type: 'echo';
+	routeSessionId: string;
+	routeThreadId: string;
+	data: {
+		echo: string;
+		sessionId: string;
+		threadId: string;
+		userId: string | null;
+	};
+}
+
+interface EchoErrorMessage {
+	type: 'error';
+	message: string;
+}
+
+type SocketMessage = EchoReadyMessage | EchoSuccessMessage | EchoErrorMessage;
+
+function createMockAuth(userId: string): AuthInterface {
+	return {
+		user: { id: userId, email: `${userId}@example.com`, name: 'Test User' },
+		session: { id: 'session-123', userId },
+		authMethod: 'session',
+		raw: {},
+		getUser: async () => ({ id: userId, email: `${userId}@example.com`, name: 'Test User' }),
+		getToken: async () => null,
+		getOrg: async () => null,
+		getOrgRole: async () => null,
+		hasOrgRole: async () => false,
+		apiKey: null,
+		hasPermission: () => false,
+	};
+}
+
+function createMockLogger(): Logger {
+	const noop = () => {};
+	return {
+		trace: noop,
+		debug: noop,
+		info: noop,
+		warn: noop,
+		error: noop,
+		fatal: noop as Logger['fatal'],
+		child: () => createMockLogger(),
+	};
+}
+
+function createMockThread(id: string): Thread {
+	const thread: Thread = {
+		id,
+		state: new Map(),
+		addEventListener: () => {},
+		removeEventListener: () => {},
+		destroy: async () => {},
+		empty: () => thread.state.size === 0,
+	};
+	return thread;
+}
+
+function createMockSession(thread: Thread, id: string): Session {
+	return {
+		id,
+		thread,
+		state: new Map(),
+		addEventListener: () => {},
+		removeEventListener: () => {},
+		serializeUserData: () => undefined,
+	};
+}
+
+function waitForOpen(socket: WebSocket): Promise<void> {
+	return new Promise((resolve, reject) => {
+		const cleanup = () => {
+			socket.removeEventListener('open', onOpen);
+			socket.removeEventListener('error', onError);
+			socket.removeEventListener('close', onClose);
+		};
+
+		const onOpen = () => {
+			cleanup();
+			resolve();
+		};
+		const onError = () => {
+			cleanup();
+			reject(new Error('WebSocket failed to open'));
+		};
+		const onClose = () => {
+			cleanup();
+			reject(new Error('WebSocket closed before opening'));
+		};
+
+		socket.addEventListener('open', onOpen, { once: true });
+		socket.addEventListener('error', onError, { once: true });
+		socket.addEventListener('close', onClose, { once: true });
+	});
+}
+
+function waitForJsonMessage(socket: WebSocket): Promise<SocketMessage> {
+	return new Promise((resolve, reject) => {
+		const cleanup = () => {
+			socket.removeEventListener('message', onMessage);
+			socket.removeEventListener('error', onError);
+			socket.removeEventListener('close', onClose);
+		};
+
+		const onMessage = (event: MessageEvent) => {
+			cleanup();
+			try {
+				resolve(JSON.parse(String(event.data)) as SocketMessage);
+			} catch (error) {
+				reject(error);
+			}
+		};
+		const onError = () => {
+			cleanup();
+			reject(new Error('WebSocket errored while waiting for a message'));
+		};
+		const onClose = () => {
+			cleanup();
+			reject(new Error('WebSocket closed before a message was received'));
+		};
+
+		socket.addEventListener('message', onMessage, { once: true });
+		socket.addEventListener('error', onError, { once: true });
+		socket.addEventListener('close', onClose, { once: true });
+	});
+}
+
+async function closeSocket(socket: WebSocket): Promise<void> {
+	if (socket.readyState === WebSocket.CLOSED) {
+		return;
+	}
+
+	await new Promise<void>((resolve) => {
+		socket.addEventListener('close', () => resolve(), { once: true });
+		socket.close();
+	});
+}
+
+describe('WebSocket agent context propagation', () => {
+	test('agent.run inside ws.onMessage preserves session, thread, and routed auth context', async () => {
+		const tracer = trace.getTracer('websocket-agent-context-test');
+
+		const echoAgent = createAgent('websocket-agent-context-propagation-test', {
+			schema: {
+				input: z.string(),
+				output: z.object({
+					echo: z.string(),
+					sessionId: z.string(),
+					threadId: z.string(),
+					userId: z.string().nullable(),
+				}),
+			},
+			handler: async (ctx, input) => {
+				return {
+					echo: input,
+					sessionId: ctx.sessionId,
+					threadId: ctx.thread.id,
+					userId: ctx.auth?.user?.id ?? null,
+				};
+			},
+		});
+
+		const app = new Hono();
+
+		app.use('*', async (c, next) => {
+			await runInHTTPContext(c, next);
+		});
+
+		app.use('/api/*', async (c, next) => {
+			const logger = createMockLogger();
+			const thread = createMockThread(`thrd_${crypto.randomUUID()}`);
+			const session = createMockSession(thread, `sess_${crypto.randomUUID()}`);
+			const waitUntilHandler = new WaitUntilHandler(tracer);
+
+			c.set('logger', logger);
+			c.set('tracer', tracer);
+			c.set('sessionId', session.id);
+			c.set('thread', thread);
+			c.set('session', session);
+			c.set('waitUntilHandler', waitUntilHandler);
+			c.set('agentIds', new Set<string>());
+			c.set('trigger', 'websocket');
+			c.set('app', {});
+			await next();
+		});
+
+		app.use('/api/*', createAgentMiddleware(''));
+
+		// This middleware runs after createAgentMiddleware('') and should still
+		// be visible to the agent via the lazy ctx.auth getter.
+		app.use('/api/*', async (c, next) => {
+			c.set('auth', createMockAuth('late-bound-user'));
+			await next();
+		});
+
+		app.get(
+			'/api/echo',
+			websocket((c, ws) => {
+				ws.onOpen(() => {
+					ws.send(JSON.stringify({ type: 'ready' }));
+				});
+
+				ws.onMessage(async (event) => {
+					try {
+						const result = await echoAgent.run(String(event.data));
+						ws.send(
+							JSON.stringify({
+								type: 'echo',
+								routeSessionId: c.var.sessionId,
+								routeThreadId: c.var.thread.id,
+								data: result,
+							})
+						);
+					} catch (error) {
+						ws.send(
+							JSON.stringify({
+								type: 'error',
+								message: error instanceof Error ? error.message : String(error),
+							})
+						);
+					}
+				});
+			})
+		);
+
+		const server = Bun.serve({
+			port: 0,
+			fetch: (request, server) => app.fetch(request, server),
+			websocket: bunWebsocket,
+		});
+
+		const socket = new WebSocket(`ws://127.0.0.1:${server.port}/api/echo`);
+
+		try {
+			await waitForOpen(socket);
+
+			const ready = await waitForJsonMessage(socket);
+			expect(ready).toEqual({ type: 'ready' });
+
+			socket.send('hello from websocket test');
+
+			const response = await waitForJsonMessage(socket);
+			if (response.type !== 'echo') {
+				throw new Error(`Expected echo response, received ${JSON.stringify(response)}`);
+			}
+
+			expect(response.data.echo).toBe('hello from websocket test');
+			expect(response.data.sessionId).toBe(response.routeSessionId);
+			expect(response.data.threadId).toBe(response.routeThreadId);
+			expect(response.data.userId).toBe('late-bound-user');
+			expect(response.data.sessionId.length).toBeGreaterThan(0);
+			expect(response.data.threadId.length).toBeGreaterThan(0);
+		} finally {
+			await closeSocket(socket);
+			server.stop(true);
+		}
+	});
+});