diff --git a/synapse/app/generic_worker.py b/synapse/app/generic_worker.py
index 4f0eefff564e..4ee4096a63da 100644
--- a/synapse/app/generic_worker.py
+++ b/synapse/app/generic_worker.py
@@ -22,7 +22,6 @@
 from typing_extensions import ContextManager
 
 from twisted.internet import defer, reactor
-from twisted.web.resource import NoResource
 
 import synapse
 import synapse.events
@@ -41,7 +40,7 @@
 from synapse.federation import send_queue
 from synapse.federation.transport.server import TransportLayerServer
 from synapse.handlers.presence import BasePresenceHandler, get_interested_parties
-from synapse.http.server import JsonResource, OptionsOnlyResource
+from synapse.http.server import JsonResource, OptionsResource
 from synapse.http.servlet import RestServlet, parse_json_object_from_request
 from synapse.http.site import SynapseSite
 from synapse.logging.context import LoggingContext
@@ -574,17 +573,7 @@ def _listen_http(self, listener_config):
                 if name == "replication":
                     resources[REPLICATION_PREFIX] = ReplicationRestResource(self)
 
-            # Avoid 404s for requests to the media repo on workers which do not
-            # have the media listener enabled.
-            if "media" not in res["names"]:
-                resources.update(
-                    {
-                        MEDIA_PREFIX: OptionsOnlyResource(),
-                        LEGACY_MEDIA_PREFIX: OptionsOnlyResource(),
-                    }
-                )
-
-        root_resource = create_resource_tree(resources, NoResource())
+        root_resource = create_resource_tree(resources, OptionsResource())
 
         _base.listen_tcp(
             bind_addresses,
diff --git a/synapse/app/homeserver.py b/synapse/app/homeserver.py
index d7f337e586ca..93a5ba2100b9 100644
--- a/synapse/app/homeserver.py
+++ b/synapse/app/homeserver.py
@@ -31,7 +31,7 @@
 from twisted.application import service
 from twisted.internet import defer, reactor
 from twisted.python.failure import Failure
-from twisted.web.resource import EncodingResourceWrapper, IResource, NoResource
+from twisted.web.resource import EncodingResourceWrapper, IResource
 from twisted.web.server import GzipEncoderFactory
 from twisted.web.static import File
 
@@ -52,7 +52,11 @@
 from synapse.config.homeserver import HomeServerConfig
 from synapse.federation.transport.server import TransportLayerServer
 from synapse.http.additional_resource import AdditionalResource
-from synapse.http.server import RootRedirect
+from synapse.http.server import (
+    OptionsResource,
+    RootOptionsRedirectResource,
+    RootRedirect,
+)
 from synapse.http.site import SynapseSite
 from synapse.logging.context import LoggingContext
 from synapse.metrics import METRICS_PREFIX, MetricsResource, RegistryProxy
@@ -121,11 +125,11 @@ def _listener_http(self, config, listener_config):
 
         # try to find something useful to redirect '/' to
         if WEB_CLIENT_PREFIX in resources:
-            root_resource = RootRedirect(WEB_CLIENT_PREFIX)
+            root_resource = RootOptionsRedirectResource(WEB_CLIENT_PREFIX)
         elif STATIC_PREFIX in resources:
-            root_resource = RootRedirect(STATIC_PREFIX)
+            root_resource = RootOptionsRedirectResource(STATIC_PREFIX)
         else:
-            root_resource = NoResource()
+            root_resource = OptionsResource()
 
         root_resource = create_resource_tree(resources, root_resource)
 
diff --git a/synapse/http/server.py b/synapse/http/server.py
index f461516d7158..33fcfbea6ee8 100644
--- a/synapse/http/server.py
+++ b/synapse/http/server.py
@@ -350,9 +350,6 @@ def _get_handler_for_request(self, request):
                 register_paths, so will return (possibly via Deferred) either
                 None, or a tuple of (http code, response body).
         """
-        if request.method == b"OPTIONS":
-            return _options_handler, "options_request_handler", {}
-
         request_path = request.path.decode("ascii")
 
         # Loop through all the registered callbacks to check if the method
@@ -404,29 +401,6 @@ def render(self, request):
         return NOT_DONE_YET
 
 
-class OptionsOnlyResource(resource.Resource):
-    """
-    A resource which responds only to OPTION requests for itself and all children.
-
-    All other requests return a 404.
-    """
-
-    def render(self, request):
-        if request.method == b"OPTIONS":
-            code, response_json_object = _options_handler(request)
-
-        else:
-            # Otherwise, 404.
-            code, response_json_object = 404, {}
-
-        return respond_with_json(
-            request, code, response_json_object, send_cors=False, canonical_json=False,
-        )
-
-    def getChild(self, name, request):
-        return self  # select ourselves as the child to render
-
-
 def _options_handler(request):
     """Request handler for OPTIONS requests
 
@@ -471,6 +445,26 @@ def getChild(self, name, request):
         return resource.Resource.getChild(self, name, request)
 
 
+class OptionsResource(resource.Resource):
+    """Responds to OPTION requests for itself and all children."""
+
+    def render_OPTIONS(self, request):
+        code, response_json_object = _options_handler(request)
+
+        return respond_with_json(
+            request, code, response_json_object, send_cors=False, canonical_json=False,
+        )
+
+    def getChildWithDefault(self, path, request):
+        if request.method == b"OPTIONS":
+            return self  # select ourselves as the child to render
+        return resource.Resource.getChildWithDefault(self, path, request)
+
+
+class RootOptionsRedirectResource(OptionsResource, RootRedirect):
+    pass
+
+
 def respond_with_json(
     request,
     code,