diff --git a/changelog.d/2380.bugfix b/changelog.d/2380.bugfix
new file mode 100644
index 000000000..eae320603
--- /dev/null
+++ b/changelog.d/2380.bugfix
@@ -0,0 +1 @@
+Return an HTTP 404 instead of 400 when requesting a filter by ID that is unknown to the server. Thanks to @krombel for contributing this!
diff --git a/synapse/rest/client/v2_alpha/filter.py b/synapse/rest/client/v2_alpha/filter.py
index c6ddf24c8..17a8bc736 100644
--- a/synapse/rest/client/v2_alpha/filter.py
+++ b/synapse/rest/client/v2_alpha/filter.py
@@ -17,7 +17,7 @@ import logging
 
 from twisted.internet import defer
 
-from synapse.api.errors import AuthError, Codes, StoreError, SynapseError
+from synapse.api.errors import AuthError, NotFoundError, StoreError, SynapseError
 from synapse.http.servlet import RestServlet, parse_json_object_from_request
 from synapse.types import UserID
 
@@ -52,13 +52,15 @@ class GetFilterRestServlet(RestServlet):
             raise SynapseError(400, "Invalid filter_id")
 
         try:
-            filter = yield self.filtering.get_user_filter(
+            filter_collection = yield self.filtering.get_user_filter(
                 user_localpart=target_user.localpart, filter_id=filter_id
             )
+        except StoreError as e:
+            if e.code != 404:
+                raise
+            raise NotFoundError("No such filter")
 
-            return 200, filter.get_filter_json()
-        except (KeyError, StoreError):
-            raise SynapseError(400, "No such filter", errcode=Codes.NOT_FOUND)
+        return 200, filter_collection.get_filter_json()
 
 
 class CreateFilterRestServlet(RestServlet):
diff --git a/synapse/rest/client/v2_alpha/sync.py b/synapse/rest/client/v2_alpha/sync.py
index c98c5a380..a883c8add 100644
--- a/synapse/rest/client/v2_alpha/sync.py
+++ b/synapse/rest/client/v2_alpha/sync.py
@@ -21,7 +21,7 @@ from canonicaljson import json
 from twisted.internet import defer
 
 from synapse.api.constants import PresenceState
-from synapse.api.errors import SynapseError
+from synapse.api.errors import Codes, StoreError, SynapseError
 from synapse.api.filtering import DEFAULT_FILTER_COLLECTION, FilterCollection
 from synapse.events.utils import (
     format_event_for_client_v2_without_room_id,
@@ -119,25 +119,32 @@ class SyncRestServlet(RestServlet):
 
         request_key = (user, timeout, since, filter_id, full_state, device_id)
 
-        if filter_id:
-            if filter_id.startswith("{"):
-                try:
-                    filter_object = json.loads(filter_id)
-                    set_timeline_upper_limit(
-                        filter_object, self.hs.config.filter_timeline_limit
-                    )
-                except Exception:
-                    raise SynapseError(400, "Invalid filter JSON")
-                self.filtering.check_valid_filter(filter_object)
-                filter = FilterCollection(filter_object)
-            else:
-                filter = yield self.filtering.get_user_filter(user.localpart, filter_id)
+        if filter_id is None:
+            filter_collection = DEFAULT_FILTER_COLLECTION
+        elif filter_id.startswith("{"):
+            try:
+                filter_object = json.loads(filter_id)
+                set_timeline_upper_limit(
+                    filter_object, self.hs.config.filter_timeline_limit
+                )
+            except Exception:
+                raise SynapseError(400, "Invalid filter JSON")
+            self.filtering.check_valid_filter(filter_object)
+            filter_collection = FilterCollection(filter_object)
         else:
-            filter = DEFAULT_FILTER_COLLECTION
+            try:
+                filter_collection = yield self.filtering.get_user_filter(
+                    user.localpart, filter_id
+                )
+            except StoreError as err:
+                if err.code != 404:
+                    raise
+                # fix up the description and errcode to be more useful
+                raise SynapseError(400, "No such filter", errcode=Codes.INVALID_PARAM)
 
         sync_config = SyncConfig(
             user=user,
-            filter_collection=filter,
+            filter_collection=filter_collection,
             is_guest=requester.is_guest,
             request_key=request_key,
             device_id=device_id,
@@ -171,7 +178,7 @@ class SyncRestServlet(RestServlet):
 
         time_now = self.clock.time_msec()
         response_content = yield self.encode_response(
-            time_now, sync_result, requester.access_token_id, filter
+            time_now, sync_result, requester.access_token_id, filter_collection
         )
 
         return 200, response_content
diff --git a/tests/rest/client/v2_alpha/test_filter.py b/tests/rest/client/v2_alpha/test_filter.py
index f42a8efbf..e0e9e94fb 100644
--- a/tests/rest/client/v2_alpha/test_filter.py
+++ b/tests/rest/client/v2_alpha/test_filter.py
@@ -92,7 +92,7 @@ class FilterTestCase(unittest.HomeserverTestCase):
         )
         self.render(request)
 
-        self.assertEqual(channel.result["code"], b"400")
+        self.assertEqual(channel.result["code"], b"404")
         self.assertEquals(channel.json_body["errcode"], Codes.NOT_FOUND)
 
     # Currently invalid params do not have an appropriate errcode