diff --git a/tests/app/test_openid_listener.py b/tests/app/test_openid_listener.py
index cf3baad96f..329aadc3d3 100644
--- a/tests/app/test_openid_listener.py
+++ b/tests/app/test_openid_listener.py
@@ -1,5 +1,5 @@
 # -*- coding: utf-8 -*-
-# Copyright 2018 New Vector Ltd
+# Copyright 2019 New Vector Ltd
 #
 # Licensed under the Apache License, Version 2.0 (the "License");
 # you may not use this file except in compliance with the License.
@@ -16,6 +16,7 @@ from mock import patch, Mock
 from parameterized import parameterized
 
 from synapse.app.federation_reader import FederationReaderServer
+from synapse.app.homeserver import SynapseHomeServer
 
 from tests.unittest import HomeserverTestCase
 
@@ -64,3 +65,49 @@ class FederationReaderOpenIDListenerTests(HomeserverTestCase):
         self.render(request)
 
         self.assertEqual(channel.code, 401)
+
+
+@patch("synapse.app.homeserver.KeyApiV2Resource", new=Mock())
+class SynapseHomeserverOpenIDListenerTests(HomeserverTestCase):
+    def make_homeserver(self, reactor, clock):
+        hs = self.setup_test_homeserver(
+            http_client=None, homeserverToUse=SynapseHomeServer,
+        )
+        return hs
+
+    @parameterized.expand([
+        (["federation"], "auth_fail"),
+        ([], "no_resource"),
+        (["openid", "federation"], "auth_fail"),
+        (["openid"], "auth_fail"),
+    ])
+    def test_openid_listener(self, names, expectation):
+        """
+        Test different openid listener configurations.
+
+        401 is success here since it means we hit the handler and auth failed.
+        """
+        config = {
+            "port": 8080,
+            "bind_addresses": ["0.0.0.0"],
+            "resources": [{"names": names}],
+        }
+
+        # Listen with the config
+        self.hs._listener_http(config, config)
+
+        # Grab the resource from the site that was told to listen
+        site = self.reactor.tcpServers[0][1]
+        try:
+            self.resource = (
+                site.resource.children[b"_matrix"].children[b"federation"].children[b"v1"]
+            )
+        except KeyError:
+            if expectation == "no_resource":
+                return
+            raise
+
+        request, channel = self.make_request("GET", "/_matrix/federation/v1/openid/userinfo")
+        self.render(request)
+
+        self.assertEqual(channel.code, 401)