diff --git a/src/index.ts b/src/index.ts
index a7bde03de..db8b62d28 100644
--- a/src/index.ts
+++ b/src/index.ts
@@ -214,6 +214,7 @@ export {
   type WebSocketHooks,
   type WebSocketPeer,
   type WebSocketMessage,
+  type WebSocketResponse,
   defineWebSocketHandler,
   defineWebSocket,
 } from "./utils/ws.ts";
diff --git a/src/utils/ws.ts b/src/utils/ws.ts
index 39df0f998..968652b17 100644
--- a/src/utils/ws.ts
+++ b/src/utils/ws.ts
@@ -2,7 +2,7 @@ import { defineHandler } from "../handler.ts";
 
 import type { Hooks as WebSocketHooks } from "crossws";
 import type { H3Event } from "../event.ts";
-import type { EventHandler } from "../types/handler.ts";
+import type { EventHandler, EventHandlerRequest, EventHandlerResponse } from "../types/handler.ts";
 
 export type {
   Hooks as WebSocketHooks,
@@ -10,6 +10,19 @@ export type {
   Peer as WebSocketPeer,
 } from "crossws";
 
+/**
+ * The `426 Upgrade Required` response returned by `defineWebSocketHandler()`
+ * for WebSocket upgrade requests, augmented with the `crossws` hooks that
+ * were attached to it. Adapters (like the crossws `serve()` plugin) read
+ * `crossws` off this response to wire up the platform-specific WebSocket
+ * upgrade.
+ *
+ * `crossws` is always the resolved hooks object: when the handler is defined
+ * with an async hooks factory, `defineWebSocketHandler()` awaits it before
+ * attaching it to the response.
+ */
+export type WebSocketResponse = Response & { crossws?: Partial<WebSocketHooks> };
+
 /**
  * Define WebSocket hooks.
  *
@@ -26,6 +39,20 @@ export function defineWebSocket(hooks: Partial<WebSocketHooks>): Partial<WebSock
   return hooks;
 }
 
+export function defineWebSocketHandler(
+  hooks: Partial<WebSocketHooks>,
+): EventHandler<EventHandlerRequest, WebSocketResponse>;
+export function defineWebSocketHandler(
+  hooks: (event: H3Event) => Partial<WebSocketHooks> | Promise<Partial<WebSocketHooks>>,
+): EventHandler<EventHandlerRequest, EventHandlerResponse<WebSocketResponse>>;
+export function defineWebSocketHandler<Http extends EventHandler>(
+  hooks: Partial<WebSocketHooks>,
+  http: Http,
+): EventHandler<EventHandlerRequest, WebSocketResponse | ReturnType<Http>>;
+export function defineWebSocketHandler<Http extends EventHandler>(
+  hooks: (event: H3Event) => Partial<WebSocketHooks> | Promise<Partial<WebSocketHooks>>,
+  http: Http,
+): EventHandler<EventHandlerRequest, EventHandlerResponse<WebSocketResponse> | ReturnType<Http>>;
 /**
  * Define WebSocket event handler.
  *
@@ -65,14 +92,14 @@ export function defineWebSocketHandler(
 
     const crossws = typeof hooks === "function" ? hooks(event) : hooks;
 
-    return Object.assign(
-      new Response("WebSocket upgrade is required.", {
-        status: 426,
-      }),
-      {
-        crossws,
-      },
-    );
+    // Async hook factories must be awaited before `crossws` is attached,
+    // otherwise the response ends up carrying an unresolved Promise instead
+    // of the hooks object. Sync hooks stay on the sync path (no wrapping).
+    if (crossws instanceof Promise) {
+      return crossws.then(toUpgradeResponse);
+    }
+
+    return toUpgradeResponse(crossws);
   });
 }
 
@@ -82,3 +109,13 @@ export function defineWebSocketHandler(
 function isWebSocketUpgrade(event: H3Event): boolean {
   return event.req.headers.get("upgrade")?.toLowerCase() === "websocket";
 }
+
+/**
+ * Build the `426 Upgrade Required` response, with the resolved `crossws`
+ * hooks attached for adapters to read.
+ */
+function toUpgradeResponse(crossws: Partial<WebSocketHooks>): WebSocketResponse {
+  return Object.assign(new Response("WebSocket upgrade is required.", { status: 426 }), {
+    crossws,
+  });
+}
diff --git a/test/unit/types.test-d.ts b/test/unit/types.test-d.ts
index ae3462eff..7c10eb2b6 100644
--- a/test/unit/types.test-d.ts
+++ b/test/unit/types.test-d.ts
@@ -1,4 +1,4 @@
-import type { H3Event } from "../../src/index.ts";
+import type { H3Event, WebSocketResponse } from "../../src/index.ts";
 import { describe, it, expectTypeOf } from "vitest";
 import {
   defineHandler,
@@ -7,6 +7,7 @@ import {
   readValidatedBody,
   getValidatedQuery,
   defineValidatedHandler,
+  defineWebSocketHandler,
 } from "../../src/index.ts";
 import { defineEventHandler } from "../../src/_deprecated.ts";
 import { z } from "zod";
@@ -152,4 +153,45 @@ describe("types", () => {
       });
     });
   });
+
+  describe("defineWebSocketHandler", () => {
+    it("exposes crossws on the returned response type without a cast", () => {
+      // https://github.com/h3js/h3/issues/1258
+      // Given a WebSocket handler defined via defineWebSocketHandler
+      const wsHandler = defineWebSocketHandler({ message: () => {} });
+      // When the handler is invoked directly (as crossws adapters do)
+      const res = wsHandler({} as H3Event);
+      // Then `crossws` must be visible on the returned type, with no `as any` cast
+      expectTypeOf(res).toHaveProperty("crossws");
+    });
+
+    it("still types the http fallback handler's return value", () => {
+      // Given a WebSocket handler with an http fallback returning a string
+      const wsHandler = defineWebSocketHandler({ message: () => {} }, () => "hello");
+      const res = wsHandler({} as H3Event);
+      // Then the returned type is the union of the WebSocket response
+      // (with `crossws` visible) and the http handler's return type —
+      // neither branch is widened away.
+      expectTypeOf(res).toExtend<string | (Response & { crossws?: unknown })>();
+      expectTypeOf(res).not.toBeUnknown();
+    });
+
+    it("types an async hooks factory's return value without a cast", async () => {
+      // Given a WebSocket handler defined with an async hooks factory
+      const wsHandler = defineWebSocketHandler(async (_event) => {
+        await Promise.resolve();
+        return { message: () => {} };
+      });
+      // When the handler is invoked directly (as crossws adapters do)
+      const res = wsHandler({} as H3Event);
+      // Then the return type must itself be the union of the sync response
+      // and a Promise of it, not just `WebSocketResponse`. Otherwise
+      // await-ing a sync-typed value would be a no-op and this assertion
+      // would pass regardless of whether the factory was actually awaited.
+      expectTypeOf(res).toEqualTypeOf<WebSocketResponse | Promise<WebSocketResponse>>();
+      // And the resolved value still exposes `crossws` with no cast.
+      const awaited = await res;
+      expectTypeOf(awaited).toHaveProperty("crossws");
+    });
+  });
 });
diff --git a/test/ws.test.ts b/test/ws.test.ts
index d0de25cef..00b413a69 100644
--- a/test/ws.test.ts
+++ b/test/ws.test.ts
@@ -47,4 +47,29 @@ describe("defineWebSocketHandler", () => {
     expect((res as Response).status).toBe(426);
     expect((res as any).crossws).toEqual(hooks);
   });
+
+  it("exposes crossws on the returned response", () => {
+    // Given a WebSocket handler defined via defineWebSocketHandler
+    const wsHandler = defineWebSocketHandler(hooks);
+    // When the handler is invoked in-process (as crossws adapters do internally)
+    const res = wsHandler({} as any);
+    // Then `res.crossws` is readable, typed, and is the exact hooks object
+    expect(res.crossws).toBe(hooks);
+  });
+
+  it("awaits an async hooks factory before attaching crossws", async () => {
+    // Given a WebSocket handler defined with an async hooks factory
+    const wsHandler = defineWebSocketHandler(async (_event) => {
+      await Promise.resolve();
+      return hooks;
+    });
+    // When the handler is invoked in-process (as crossws adapters do internally)
+    // Then the return type already reflects the Promise branch, no cast needed
+    const res = await wsHandler({} as any);
+    expect(res).toBeInstanceOf(Response);
+    expect(res.status).toBe(426);
+    // Then `crossws` is the resolved hooks object, not an unresolved Promise
+    expect(res.crossws).not.toBeInstanceOf(Promise);
+    expect(res.crossws).toEqual(hooks);
+  });
 });