diff --git a/synapse/crypto/context_factory.py b/synapse/crypto/context_factory.py
index 4f48e8e88d..06e63a96b5 100644
--- a/synapse/crypto/context_factory.py
+++ b/synapse/crypto/context_factory.py
@@ -31,6 +31,7 @@ from twisted.internet.ssl import (
     platformTrust,
 )
 from twisted.python.failure import Failure
+from twisted.web.iweb import IPolicyForHTTPS
 
 logger = logging.getLogger(__name__)
 
@@ -74,6 +75,7 @@ class ServerContextFactory(ContextFactory):
         return self._context
 
 
+@implementer(IPolicyForHTTPS)
 class ClientTLSOptionsFactory(object):
     """Factory for Twisted SSLClientConnectionCreators that are used to make connections
     to remote servers for federation.
@@ -146,6 +148,12 @@ class ClientTLSOptionsFactory(object):
             f = Failure()
             tls_protocol.failVerification(f)
 
+    def creatorForNetloc(self, hostname, port):
+        """Implements the IPolicyForHTTPS interace so that this can be passed
+        directly to agents.
+        """
+        return self.get_options(hostname)
+
 
 @implementer(IOpenSSLClientConnectionCreator)
 class SSLClientConnectionCreator(object):
diff --git a/synapse/http/federation/matrix_federation_agent.py b/synapse/http/federation/matrix_federation_agent.py
index c03ddb724f..a0d5139839 100644
--- a/synapse/http/federation/matrix_federation_agent.py
+++ b/synapse/http/federation/matrix_federation_agent.py
@@ -64,10 +64,6 @@ class MatrixFederationAgent(object):
         tls_client_options_factory (ClientTLSOptionsFactory|None):
             factory to use for fetching client tls options, or none to disable TLS.
 
-        _well_known_tls_policy (IPolicyForHTTPS|None):
-            TLS policy to use for fetching .well-known files. None to use a default
-            (browser-like) implementation.
-
         _srv_resolver (SrvResolver|None):
             SRVResolver impl to use for looking up SRV records. None to use a default
             implementation.
@@ -81,7 +77,6 @@ class MatrixFederationAgent(object):
         self,
         reactor,
         tls_client_options_factory,
-        _well_known_tls_policy=None,
         _srv_resolver=None,
         _well_known_cache=well_known_cache,
     ):
@@ -98,13 +93,12 @@ class MatrixFederationAgent(object):
         self._pool.maxPersistentPerHost = 5
         self._pool.cachedConnectionTimeout = 2 * 60
 
-        agent_args = {}
-        if _well_known_tls_policy is not None:
-            # the param is called 'contextFactory', but actually passing a
-            # contextfactory is deprecated, and it expects an IPolicyForHTTPS.
-            agent_args["contextFactory"] = _well_known_tls_policy
         _well_known_agent = RedirectAgent(
-            Agent(self._reactor, pool=self._pool, **agent_args)
+            Agent(
+                self._reactor,
+                pool=self._pool,
+                contextFactory=tls_client_options_factory,
+            )
         )
         self._well_known_agent = _well_known_agent
 
diff --git a/tests/http/federation/test_matrix_federation_agent.py b/tests/http/federation/test_matrix_federation_agent.py
index b906686b49..4255add097 100644
--- a/tests/http/federation/test_matrix_federation_agent.py
+++ b/tests/http/federation/test_matrix_federation_agent.py
@@ -75,7 +75,6 @@ class MatrixFederationAgentTests(TestCase):
 
         config_dict = default_config("test", parse=False)
         config_dict["federation_custom_ca_list"] = [get_test_ca_cert_file()]
-        # config_dict["trusted_key_servers"] = []
 
         self._config = config = HomeServerConfig()
         config.parse_config_dict(config_dict, "", "")
@@ -83,7 +82,6 @@ class MatrixFederationAgentTests(TestCase):
         self.agent = MatrixFederationAgent(
             reactor=self.reactor,
             tls_client_options_factory=ClientTLSOptionsFactory(config),
-            _well_known_tls_policy=TrustingTLSPolicyForHTTPS(),
             _srv_resolver=self.mock_resolver,
             _well_known_cache=self.well_known_cache,
         )
@@ -691,16 +689,18 @@ class MatrixFederationAgentTests(TestCase):
         not signed by a CA
         """
 
-        # we use the same test server as the other tests, but use an agent
-        # with _well_known_tls_policy left to the default, which will not
-        # trust it (since the presented cert is signed by a test CA)
+        # we use the same test server as the other tests, but use an agent with
+        # the config left to the default, which will not trust it (since the
+        # presented cert is signed by a test CA)
 
         self.mock_resolver.resolve_service.side_effect = lambda _: []
         self.reactor.lookups["testserv"] = "1.2.3.4"
 
+        config = default_config("test", parse=True)
+
         agent = MatrixFederationAgent(
             reactor=self.reactor,
-            tls_client_options_factory=ClientTLSOptionsFactory(self._config),
+            tls_client_options_factory=ClientTLSOptionsFactory(config),
             _srv_resolver=self.mock_resolver,
             _well_known_cache=self.well_known_cache,
         )