diff --git a/changelog.d/12699.misc b/changelog.d/12699.misc
new file mode 100644
index 000000000..d278a956c
--- /dev/null
+++ b/changelog.d/12699.misc
@@ -0,0 +1 @@
+Respect the `@cancellable` flag for `RestServlet`s and `BaseFederationServlet`s.
diff --git a/synapse/http/server.py b/synapse/http/server.py
index f6d4d8db8..756c6e1ae 100644
--- a/synapse/http/server.py
+++ b/synapse/http/server.py
@@ -314,6 +314,9 @@ class HttpServer(Protocol):
         If the regex contains groups these gets passed to the callback via
         an unpacked tuple.
 
+        The callback may be marked with the `@cancellable` decorator, which will
+        cause request processing to be cancelled when clients disconnect early.
+
         Args:
             method: The HTTP method to listen to.
             path_patterns: The regex used to match requests.
@@ -544,6 +547,8 @@ class JsonResource(DirectServeJsonResource):
     async def _async_render(self, request: SynapseRequest) -> Tuple[int, Any]:
         callback, servlet_classname, group_dict = self._get_handler_for_request(request)
 
+        request.is_render_cancellable = is_method_cancellable(callback)
+
         # Make sure we have an appropriate name for this handler in prometheus
         # (rather than the default of JsonResource).
         request.request_metrics.name = servlet_classname
diff --git a/tests/federation/transport/server/__init__.py b/tests/federation/transport/server/__init__.py
new file mode 100644
index 000000000..3a5f22c02
--- /dev/null
+++ b/tests/federation/transport/server/__init__.py
@@ -0,0 +1,13 @@
+# Copyright 2022 The Matrix.org Foundation C.I.C.
+#
+# Licensed under the Apache License, Version 2.0 (the "License");
+# you may not use this file except in compliance with the License.
+# You may obtain a copy of the License at
+#
+#     http://www.apache.org/licenses/LICENSE-2.0
+#
+# Unless required by applicable law or agreed to in writing, software
+# distributed under the License is distributed on an "AS IS" BASIS,
+# WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+# See the License for the specific language governing permissions and
+# limitations under the License.
diff --git a/tests/federation/transport/server/test__base.py b/tests/federation/transport/server/test__base.py
new file mode 100644
index 000000000..98a951f03
--- /dev/null
+++ b/tests/federation/transport/server/test__base.py
@@ -0,0 +1,112 @@
+# Copyright 2022 The Matrix.org Foundation C.I.C.
+#
+# Licensed under the Apache License, Version 2.0 (the "License");
+# you may not use this file except in compliance with the License.
+# You may obtain a copy of the License at
+#
+#     http://www.apache.org/licenses/LICENSE-2.0
+#
+# Unless required by applicable law or agreed to in writing, software
+# distributed under the License is distributed on an "AS IS" BASIS,
+# WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+# See the License for the specific language governing permissions and
+# limitations under the License.
+
+from http import HTTPStatus
+from typing import Dict, List, Tuple
+
+from synapse.api.errors import Codes
+from synapse.federation.transport.server import BaseFederationServlet
+from synapse.federation.transport.server._base import Authenticator
+from synapse.http.server import JsonResource, cancellable
+from synapse.server import HomeServer
+from synapse.types import JsonDict
+from synapse.util.ratelimitutils import FederationRateLimiter
+
+from tests import unittest
+from tests.http.server._base import EndpointCancellationTestHelperMixin
+
+
+class CancellableFederationServlet(BaseFederationServlet):
+    PATH = "/sleep"
+
+    def __init__(
+        self,
+        hs: HomeServer,
+        authenticator: Authenticator,
+        ratelimiter: FederationRateLimiter,
+        server_name: str,
+    ):
+        super().__init__(hs, authenticator, ratelimiter, server_name)
+        self.clock = hs.get_clock()
+
+    @cancellable
+    async def on_GET(
+        self, origin: str, content: None, query: Dict[bytes, List[bytes]]
+    ) -> Tuple[int, JsonDict]:
+        await self.clock.sleep(1.0)
+        return HTTPStatus.OK, {"result": True}
+
+    async def on_POST(
+        self, origin: str, content: JsonDict, query: Dict[bytes, List[bytes]]
+    ) -> Tuple[int, JsonDict]:
+        await self.clock.sleep(1.0)
+        return HTTPStatus.OK, {"result": True}
+
+
+class BaseFederationServletCancellationTests(
+    unittest.FederatingHomeserverTestCase, EndpointCancellationTestHelperMixin
+):
+    """Tests for `BaseFederationServlet` cancellation."""
+
+    path = f"{CancellableFederationServlet.PREFIX}{CancellableFederationServlet.PATH}"
+
+    def create_test_resource(self):
+        """Overrides `HomeserverTestCase.create_test_resource`."""
+        resource = JsonResource(self.hs)
+
+        CancellableFederationServlet(
+            hs=self.hs,
+            authenticator=Authenticator(self.hs),
+            ratelimiter=self.hs.get_federation_ratelimiter(),
+            server_name=self.hs.hostname,
+        ).register(resource)
+
+        return resource
+
+    def test_cancellable_disconnect(self) -> None:
+        """Test that handlers with the `@cancellable` flag can be cancelled."""
+        channel = self.make_signed_federation_request(
+            "GET", self.path, await_result=False
+        )
+
+        # Advance past all the rate limiting logic. If we disconnect too early, the
+        # request won't be processed.
+        self.pump()
+
+        self._test_disconnect(
+            self.reactor,
+            channel,
+            expect_cancellation=True,
+            expected_body={"error": "Request cancelled", "errcode": Codes.UNKNOWN},
+        )
+
+    def test_uncancellable_disconnect(self) -> None:
+        """Test that handlers without the `@cancellable` flag cannot be cancelled."""
+        channel = self.make_signed_federation_request(
+            "POST",
+            self.path,
+            content={},
+            await_result=False,
+        )
+
+        # Advance past all the rate limiting logic. If we disconnect too early, the
+        # request won't be processed.
+        self.pump()
+
+        self._test_disconnect(
+            self.reactor,
+            channel,
+            expect_cancellation=False,
+            expected_body={"result": True},
+        )
diff --git a/tests/http/test_servlet.py b/tests/http/test_servlet.py
index a80bfb9f4..ad521525c 100644
--- a/tests/http/test_servlet.py
+++ b/tests/http/test_servlet.py
@@ -12,16 +12,25 @@
 # See the License for the specific language governing permissions and
 # limitations under the License.
 import json
+from http import HTTPStatus
 from io import BytesIO
+from typing import Tuple
 from unittest.mock import Mock
 
-from synapse.api.errors import SynapseError
+from synapse.api.errors import Codes, SynapseError
+from synapse.http.server import cancellable
 from synapse.http.servlet import (
+    RestServlet,
     parse_json_object_from_request,
     parse_json_value_from_request,
 )
+from synapse.http.site import SynapseRequest
+from synapse.rest.client._base import client_patterns
+from synapse.server import HomeServer
+from synapse.types import JsonDict
 
 from tests import unittest
+from tests.http.server._base import EndpointCancellationTestHelperMixin
 
 
 def make_request(content):
@@ -76,3 +85,52 @@ class TestServletUtils(unittest.TestCase):
         # Test not an object
         with self.assertRaises(SynapseError):
             parse_json_object_from_request(make_request(b'["foo"]'))
+
+
+class CancellableRestServlet(RestServlet):
+    """A `RestServlet` with a mix of cancellable and uncancellable handlers."""
+
+    PATTERNS = client_patterns("/sleep$")
+
+    def __init__(self, hs: HomeServer):
+        super().__init__()
+        self.clock = hs.get_clock()
+
+    @cancellable
+    async def on_GET(self, request: SynapseRequest) -> Tuple[int, JsonDict]:
+        await self.clock.sleep(1.0)
+        return HTTPStatus.OK, {"result": True}
+
+    async def on_POST(self, request: SynapseRequest) -> Tuple[int, JsonDict]:
+        await self.clock.sleep(1.0)
+        return HTTPStatus.OK, {"result": True}
+
+
+class TestRestServletCancellation(
+    unittest.HomeserverTestCase, EndpointCancellationTestHelperMixin
+):
+    """Tests for `RestServlet` cancellation."""
+
+    servlets = [
+        lambda hs, http_server: CancellableRestServlet(hs).register(http_server)
+    ]
+
+    def test_cancellable_disconnect(self) -> None:
+        """Test that handlers with the `@cancellable` flag can be cancelled."""
+        channel = self.make_request("GET", "/sleep", await_result=False)
+        self._test_disconnect(
+            self.reactor,
+            channel,
+            expect_cancellation=True,
+            expected_body={"error": "Request cancelled", "errcode": Codes.UNKNOWN},
+        )
+
+    def test_uncancellable_disconnect(self) -> None:
+        """Test that handlers without the `@cancellable` flag cannot be cancelled."""
+        channel = self.make_request("POST", "/sleep", await_result=False)
+        self._test_disconnect(
+            self.reactor,
+            channel,
+            expect_cancellation=False,
+            expected_body={"result": True},
+        )
diff --git a/tests/unittest.py b/tests/unittest.py
index 9afa68c16..e7f255b4f 100644
--- a/tests/unittest.py
+++ b/tests/unittest.py
@@ -831,7 +831,7 @@ class FederatingHomeserverTestCase(HomeserverTestCase):
             self.site,
             method=method,
             path=path,
-            content=content or "",
+            content=content if content is not None else "",
             shorthand=False,
             await_result=await_result,
             custom_headers=custom_headers,