diff --git a/synapse/http/matrixfederationclient.py b/synapse/http/matrixfederationclient.py
index 6b41639741..b27c4c1c38 100644
--- a/synapse/http/matrixfederationclient.py
+++ b/synapse/http/matrixfederationclient.py
@@ -238,10 +238,10 @@ class MatrixFederationHttpClient(object):
             # Enable backoff if initially disabled
             send_request_args["backoff_on_404"] = backoff_on_404
 
-            send_request_args["path"] += "/"
+            # Add trailing slash
+            send_request_args["request"].path += "/"
 
             response = yield self._send_request(**send_request_args)
-
             body = yield _handle_json_response(
                 self.hs.get_reactor(), self.default_timeout, request, response,
             )
diff --git a/tests/http/test_fedclient.py b/tests/http/test_fedclient.py
index b03b37affe..b45eee3a82 100644
--- a/tests/http/test_fedclient.py
+++ b/tests/http/test_fedclient.py
@@ -268,6 +268,60 @@ class FederationClientTests(HomeserverTestCase):
 
         self.assertIsInstance(f.value, TimeoutError)
 
+    def test_client_requires_trailing_slashes(self):
+        """
+        If a connection is made to a client but the client rejects it due to
+        requiring a trailing slash. We need to retry the request with a
+        trailing slash. Workaround for Synapse <=v0.99.2, explained in #3622.
+        """
+        d = self.cl.get_json(
+            "testserv:8008", "foo/bar", try_trailing_slash_on_400=True,
+        )
+
+        self.pump()
+
+        # there should have been a call to connectTCP
+        clients = self.reactor.tcpClients
+        self.assertEqual(len(clients), 1)
+        (_host, _port, factory, _timeout, _bindAddress) = clients[0]
+
+        # complete the connection and wire it up to a fake transport
+        client = factory.buildProtocol(None)
+        conn = StringTransport()
+        client.makeConnection(conn)
+
+        # that should have made it send the request to the connection
+        self.assertRegex(conn.value(), b"^GET /foo/bar")
+
+        # Send the HTTP response
+        client.dataReceived(
+            b"HTTP/1.1 400 Bad Request\r\n"
+            b"Content-Type: application/json\r\n"
+            b"Content-Length: 59\r\n"
+            b"\r\n"
+            b'{"errcode":"M_UNRECOGNIZED","error":"Unrecognized request"}'
+        )
+
+        # We should get a 400 response, then try again
+        self.pump()
+
+        # We should get another request wiht a trailing slash
+        self.assertRegex(conn.value(), b"^GET /foo/bar/")
+
+        # Send a happy response this time
+        client.dataReceived(
+            b"HTTP/1.1 200 OK\r\n"
+            b"Content-Type: application/json\r\n"
+            b"Content-Length: 2\r\n"
+            b"\r\n"
+            b'{}'
+        )
+
+        # We should get a successful response
+        r = self.successResultOf(d)
+        self.assertEqual(r.code, 200)
+        self.assertEqual(r, {})
+
     def test_client_sends_body(self):
         self.cl.post_json(
             "testserv:8008", "foo/bar", timeout=10000,