diff --git a/CHANGELOG.md b/CHANGELOG.md
index 2fb24b979c..8c147d0a5c 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -25,6 +25,7 @@ This project adheres to [Semantic Versioning](https://semver.org/).
 - [#3986](https://github.com/plotly/dash/pull/3986) Adjust `_run_before_hooks` in the `fastapi` backend to honor a response returned by a `before_request` function, matching the `flask` backend's behavior.
 
 ### Fixed
+- [#4027](https://github.com/plotly/dash/pull/4027) Support `async def` hook routes (`dash.hooks.route`) on all backends, stop hook routes from leaking the app context to the caller, and let hook routes and MCP read the request on the `fastapi` backend.
 - [#3980](https://github.com/plotly/dash/pull/3980) Fix the three `before_request` hooks (`Dash._setup_server` and the pages `router_sync` / `router_async`) publishing their "already done" guard flag before the setup work behind it had run. Under a multi-threaded WSGI worker such as `gunicorn -k gthread` (or under an ASGI worker for the async router), a second request arriving mid-setup could observe the flag already set, skip setup, then read `registered_paths` / `callback_map` / the pages router callback while they were still being registered - causing the first burst of component bundle requests after a restart to 500 with `Error loading dependency. "<lib>" is not a registered library`, or the pages router to hit `DuplicateCallback` when two workers raced past the guard. Each hook body now runs under a lock (`threading.Lock` for the two sync hooks, an `asyncio.Lock` bound to the running loop for the async router) and only publishes the flag after all work completes. Fixes [#3971](https://github.com/plotly/dash/issues/3971).
 - [#3944](https://github.com/plotly/dash/pull/3944) Fix `dash.testing` runner backend detection for wrapped FastAPI/Quart servers so threaded Flask-only options are not passed to ASGI runners.
 - [#3955](https://github.com/plotly/dash/pull/3955) Unpin `selenium` in the testing requirements (was capped at `<=4.2.0` from 2022) and require `>=4.11.0`, so it can drive current stable Chrome via Selenium Manager and stop the widespread CI flakiness.
diff --git a/dash/_get_app.py b/dash/_get_app.py
index ab0b897f81..3c6f8c2310 100644
--- a/dash/_get_app.py
+++ b/dash/_get_app.py
@@ -1,4 +1,5 @@
 import functools
+import inspect
 
 from contextvars import ContextVar, copy_context
 from textwrap import dedent
@@ -32,10 +33,25 @@ async def wrap(self, *args, **kwargs):
 
 
 def with_app_context_factory(func, app):
+    if inspect.iscoroutinefunction(func):
+
+        @functools.wraps(func)
+        async def async_wrap(*args, **kwargs):
+            # The coroutine runs in the awaiting task's context, so set the app
+            # there and restore it after, rather than in a copied context.
+            token = app_context.set(app)
+            try:
+                return await func(*args, **kwargs)
+            finally:
+                app_context.reset(token)
+
+        return async_wrap
+
     @functools.wraps(func)
     def wrap(*args, **kwargs):
-        app_context.set(app)
+        # Set the app in the copy only, so it doesn't leak to the caller.
         ctx = copy_context()
+        ctx.run(app_context.set, app)
         return ctx.run(func, *args, **kwargs)
 
     return wrap
diff --git a/dash/_hooks.py b/dash/_hooks.py
index f260b1fcb0..8a1504f3d1 100644
--- a/dash/_hooks.py
+++ b/dash/_hooks.py
@@ -126,6 +126,10 @@ def route(
     ):
         """
         Add a route to the Dash server.
+
+        The route function can be `async def`; with the Flask backend this
+        requires `flask[async]`. Read the request with
+        `dash.get_app().backend.request_adapter()`.
         """
 
         def wrap(func: _t.Callable[[], _t.Any]):
diff --git a/dash/backends/_fastapi.py b/dash/backends/_fastapi.py
index 210f942a39..5e72f65570 100644
--- a/dash/backends/_fastapi.py
+++ b/dash/backends/_fastapi.py
@@ -148,6 +148,20 @@ def get_current_request() -> Request:
 _ENV_CONFIG = "_DASH_FASTAPI_CONFIG"
 
 
+def _replay_body(body: bytes, receive: Receive) -> Receive:
+    """ASGI receive that sends an already read request body once."""
+    sent = False
+
+    async def replay():
+        nonlocal sent
+        if not sent:
+            sent = True
+            return {"type": "http.request", "body": body, "more_body": False}
+        return await receive()
+
+    return replay
+
+
 class DashMiddleware:  # pylint: disable=too-few-public-methods
     """Consolidated middleware for all Dash/FastAPI integration needs."""
 
@@ -176,22 +190,24 @@ async def _initialize_dev_tools(self) -> None:
                 self.dash_app.enable_dev_tools(**config, first_run=False)
             self._dev_tools_initialized = True
 
-    async def _setup_timing(self, request: Request) -> None:
-        """Set up timing information for the request."""
+    async def _setup_timing(self, request: Request) -> bytes | None:
+        """Set up timing information for the request.
+
+        Returns the request body when it had to be read to parse the JSON.
+        """
+        body = None
+        request.state.json_body = None
         try:
-            request.state.json_body = (
-                await request.json()
-                if request.headers.get("content-type", "").startswith(
-                    "application/json"
-                )
-                else None
-            )
+            if request.headers.get("content-type", "").startswith("application/json"):
+                body = await request.body()
+                request.state.json_body = json.loads(body)
         except Exception:  # pylint: disable=broad-exception-caught
             request.state.json_body = None
         if self.enable_timing:
             request.state.timing_information = {
                 "__dash_server": {"dur": time.time(), "desc": None}
             }
+        return body
 
     async def _run_before_hooks(self) -> None:
         """Run all before-request hooks."""
@@ -270,7 +286,8 @@ async def _receive_with_shutdown():
             await self.app(scope, receive, send)
             return
 
-        # Non-Dash routes pass through to avoid consuming body stream
+        # Non-Dash routes pass through to avoid consuming body stream.
+        # Routes registered through Dash (hook routes, MCP) are Dash routes too.
         path = scope["path"]
         prefix = self.dash_app.config.routes_pathname_prefix
         dash_prefix = prefix.rstrip("/") + "/_dash-"
@@ -278,6 +295,7 @@ async def _receive_with_shutdown():
             not path.startswith(dash_prefix)
             and path != prefix
             and path != prefix.rstrip("/")
+            and path not in self.dash_app.routes
         ):
             await self.app(scope, receive, send)
             return
@@ -287,9 +305,12 @@ async def _receive_with_shutdown():
         token = set_current_request(request)
 
         try:
-            await self._setup_timing(request)
+            body = await self._setup_timing(request)
             await self._run_before_hooks()
 
+            if body is not None:
+                # The body stream is consumed, replay it for handlers reading it.
+                receive = _replay_body(body, receive)
             await self.app(scope, receive, send)
 
             await self._run_after_hooks()
diff --git a/tests/backend_tests/test_hook_routes.py b/tests/backend_tests/test_hook_routes.py
new file mode 100644
index 0000000000..813af55468
--- /dev/null
+++ b/tests/backend_tests/test_hook_routes.py
@@ -0,0 +1,99 @@
+"""Hook routes on every backend: sync and async views reading the request
+through the backend's request adapter, and FastAPI handlers reading the body
+themselves after the Dash middleware parsed it."""
+import asyncio
+import inspect
+
+import pytest
+
+from dash import Dash, get_app, hooks, html
+
+
+@pytest.fixture(autouse=True)
+def routes_cleanup():
+    yield
+    hooks._ns["routes"] = []
+    hooks._ns["setup"] = []
+
+
+@pytest.fixture(params=["flask", "quart", "fastapi"])
+def backend(request):
+    if request.param != "flask":
+        pytest.importorskip(request.param)
+    return request.param
+
+
+def post(app, path, body):
+    """POST JSON with the test client of the app's backend."""
+    server_type = app.backend.server_type
+    if server_type == "fastapi":
+        from starlette.testclient import TestClient
+
+        with TestClient(app.server) as client:
+            response = client.post(path, json=body)
+            return response.status_code, response.json()
+
+    if server_type == "quart":
+
+        async def run():
+            response = await app.server.test_client().post(path, json=body)
+            return response.status_code, await response.get_json()
+
+        return asyncio.run(run())
+
+    response = app.server.test_client().post(path, json=body)
+    return response.status_code, response.get_json()
+
+
+def make_app(backend):
+    app = Dash(__name__, backend=backend)
+    app.layout = html.Div()
+    return app
+
+
+def test_hook_route_sync(backend):
+    if backend == "quart":
+        pytest.skip("Quart's request adapter get_json is async")
+
+    @hooks.route("sync_echo", methods=("POST",))
+    def sync_echo():
+        adapter = get_app().backend.request_adapter()
+        return get_app().backend.jsonify({"echo": adapter.get_json()})
+
+    assert post(make_app(backend), "/sync_echo", {"a": 1}) == (200, {"echo": {"a": 1}})
+
+
+def test_hook_route_async(backend):
+    if backend == "flask":
+        pytest.importorskip("asgiref")
+
+    @hooks.route("async_echo", methods=("POST",))
+    async def async_echo():
+        app = get_app()
+        data = app.backend.request_adapter().get_json()
+        if inspect.isawaitable(data):
+            data = await data
+        return app.backend.jsonify({"echo": data, "title": app.title})
+
+    app = make_app(backend)
+    app.title = "hook app"
+    # get_app() must return the app serving the request, not the last created.
+    make_app(backend).title = "other app"
+    assert post(app, "/async_echo", {"a": 1}) == (
+        200,
+        {"echo": {"a": 1}, "title": "hook app"},
+    )
+
+
+def test_fastapi_route_reads_own_body():
+    pytest.importorskip("fastapi")
+    from starlette.requests import Request
+
+    @hooks.setup()
+    def add_route(app):
+        async def own_body(request: Request):
+            return app.backend.jsonify({"own": await request.json()})
+
+        app._add_url("own_body", own_body, ["POST"])
+
+    assert post(make_app("fastapi"), "/own_body", {"a": 1}) == (200, {"own": {"a": 1}})
diff --git a/tests/integration/test_hooks.py b/tests/integration/test_hooks.py
index 518439d819..c244c04f3d 100644
--- a/tests/integration/test_hooks.py
+++ b/tests/integration/test_hooks.py
@@ -10,7 +10,7 @@ def hook_cleanup():
     yield
     hooks._ns["layout"] = []
     hooks._ns["setup"] = []
-    hooks._ns["route"] = []
+    hooks._ns["routes"] = []
     hooks._ns["error"] = []
     hooks._ns["callback"] = []
     hooks._ns["index"] = []