diff --git a/changelog.d/11602.bugfix b/changelog.d/11602.bugfix
new file mode 100644
index 000000000000..e0dfbf1a1520
--- /dev/null
+++ b/changelog.d/11602.bugfix
@@ -0,0 +1 @@
+Fix a long-standing bug that some unknown endpoints would return HTML error pages instead of JSON `M_UNRECOGNIZED` errors.
diff --git a/synapse/app/homeserver.py b/synapse/app/homeserver.py
index dd76e0732108..177ce040e857 100644
--- a/synapse/app/homeserver.py
+++ b/synapse/app/homeserver.py
@@ -27,6 +27,7 @@
 import synapse.config.logger
 from synapse import events
 from synapse.api.urls import (
+    CLIENT_API_PREFIX,
     FEDERATION_PREFIX,
     LEGACY_MEDIA_PREFIX,
     MEDIA_R0_PREFIX,
@@ -192,13 +193,7 @@ def _configure_named_resource(
 
             resources.update(
                 {
-                    "/_matrix/client/api/v1": client_resource,
-                    "/_matrix/client/r0": client_resource,
-                    "/_matrix/client/v1": client_resource,
-                    "/_matrix/client/v3": client_resource,
-                    "/_matrix/client/unstable": client_resource,
-                    "/_matrix/client/v2_alpha": client_resource,
-                    "/_matrix/client/versions": client_resource,
+                    CLIENT_API_PREFIX: client_resource,
                     "/.well-known": well_known_resource(self),
                     "/_synapse/admin": AdminRestResource(self),
                     **build_synapse_client_resource_tree(self),
diff --git a/synapse/http/server.py b/synapse/http/server.py
index 4fd5660a0819..7bbbe7648b8f 100644
--- a/synapse/http/server.py
+++ b/synapse/http/server.py
@@ -530,7 +530,7 @@ class RootRedirect(resource.Resource):
     """Redirects the root '/' path to another path."""
 
     def __init__(self, path: str):
-        resource.Resource.__init__(self)
+        super().__init__()
         self.url = path
 
     def render_GET(self, request: Request) -> bytes:
@@ -539,7 +539,7 @@ def render_GET(self, request: Request) -> bytes:
     def getChild(self, name: str, request: Request) -> resource.Resource:
         if len(name) == 0:
             return self  # select ourselves as the child to render
-        return resource.Resource.getChild(self, name, request)
+        return super().getChild(name, request)
 
 
 class OptionsResource(resource.Resource):
@@ -556,7 +556,7 @@ def render_OPTIONS(self, request: Request) -> bytes:
     def getChildWithDefault(self, path: str, request: Request) -> resource.Resource:
         if request.method == b"OPTIONS":
             return self  # select ourselves as the child to render
-        return resource.Resource.getChildWithDefault(self, path, request)
+        return super().getChildWithDefault(path, request)
 
 
 class RootOptionsRedirectResource(OptionsResource, RootRedirect):