diff --git a/synapse/api/auth.py b/synapse/api/auth.py
index a4d658a9d..521a52e00 100644
--- a/synapse/api/auth.py
+++ b/synapse/api/auth.py
@@ -629,7 +629,10 @@ class Auth(object):
         except AuthError:
             # TODO(daniel): Remove this fallback when all existing access tokens
             # have been re-issued as macaroons.
+            if self.hs.config.expire_access_token:
+                raise
             ret = yield self._look_up_user_by_access_token(token)
+
         defer.returnValue(ret)
 
     @defer.inlineCallbacks
diff --git a/synapse/handlers/auth.py b/synapse/handlers/auth.py
index e259213a3..5a0ed9d6b 100644
--- a/synapse/handlers/auth.py
+++ b/synapse/handlers/auth.py
@@ -637,12 +637,13 @@ class AuthHandler(BaseHandler):
         yield self.store.add_refresh_token_to_user(user_id, refresh_token)
         defer.returnValue(refresh_token)
 
-    def generate_access_token(self, user_id, extra_caveats=None):
+    def generate_access_token(self, user_id, extra_caveats=None,
+                              duration_in_ms=(60 * 60 * 1000)):
         extra_caveats = extra_caveats or []
         macaroon = self._generate_base_macaroon(user_id)
         macaroon.add_first_party_caveat("type = access")
         now = self.hs.get_clock().time_msec()
-        expiry = now + (60 * 60 * 1000)
+        expiry = now + duration_in_ms
         macaroon.add_first_party_caveat("time < %d" % (expiry,))
         for caveat in extra_caveats:
             macaroon.add_first_party_caveat(caveat)
diff --git a/synapse/handlers/register.py b/synapse/handlers/register.py
index 8c3381df8..6b33b2714 100644
--- a/synapse/handlers/register.py
+++ b/synapse/handlers/register.py
@@ -360,7 +360,7 @@ class RegistrationHandler(BaseHandler):
         defer.returnValue(data)
 
     @defer.inlineCallbacks
-    def get_or_create_user(self, localpart, displayname, duration_seconds,
+    def get_or_create_user(self, localpart, displayname, duration_in_ms,
                            password_hash=None):
         """Creates a new user if the user does not exist,
         else revokes all previous access tokens and generates a new one.
@@ -390,8 +390,8 @@ class RegistrationHandler(BaseHandler):
 
         user = UserID(localpart, self.hs.hostname)
         user_id = user.to_string()
-        token = self.auth_handler().generate_short_term_login_token(
-            user_id, duration_seconds)
+        token = self.auth_handler().generate_access_token(
+            user_id, None, duration_in_ms)
 
         if need_register:
             yield self.store.register(
diff --git a/synapse/rest/client/v1/register.py b/synapse/rest/client/v1/register.py
index ce7099b18..8e1f1b784 100644
--- a/synapse/rest/client/v1/register.py
+++ b/synapse/rest/client/v1/register.py
@@ -429,7 +429,7 @@ class CreateUserRestServlet(ClientV1RestServlet):
         user_id, token = yield handler.get_or_create_user(
             localpart=localpart,
             displayname=displayname,
-            duration_seconds=duration_seconds,
+            duration_in_ms=(duration_seconds * 1000),
             password_hash=password_hash
         )
 
diff --git a/tests/api/test_auth.py b/tests/api/test_auth.py
index ad269af0e..960c23d63 100644
--- a/tests/api/test_auth.py
+++ b/tests/api/test_auth.py
@@ -281,7 +281,7 @@ class AuthTestCase(unittest.TestCase):
         macaroon.add_first_party_caveat("gen = 1")
         macaroon.add_first_party_caveat("type = access")
         macaroon.add_first_party_caveat("user_id = %s" % (user,))
-        macaroon.add_first_party_caveat("time < 1")  # ms
+        macaroon.add_first_party_caveat("time < -2000")  # ms
 
         self.hs.clock.now = 5000  # seconds
         self.hs.config.expire_access_token = True
@@ -293,3 +293,32 @@ class AuthTestCase(unittest.TestCase):
             yield self.auth.get_user_from_macaroon(macaroon.serialize())
         self.assertEqual(401, cm.exception.code)
         self.assertIn("Invalid macaroon", cm.exception.msg)
+
+    @defer.inlineCallbacks
+    def test_get_user_from_macaroon_with_valid_duration(self):
+        # TODO(danielwh): Remove this mock when we remove the
+        # get_user_by_access_token fallback.
+        self.store.get_user_by_access_token = Mock(
+            return_value={"name": "@baldrick:matrix.org"}
+        )
+
+        self.store.get_user_by_access_token = Mock(
+            return_value={"name": "@baldrick:matrix.org"}
+        )
+
+        user_id = "@baldrick:matrix.org"
+        macaroon = pymacaroons.Macaroon(
+            location=self.hs.config.server_name,
+            identifier="key",
+            key=self.hs.config.macaroon_secret_key)
+        macaroon.add_first_party_caveat("gen = 1")
+        macaroon.add_first_party_caveat("type = access")
+        macaroon.add_first_party_caveat("user_id = %s" % (user_id,))
+        macaroon.add_first_party_caveat("time < 900000000")  # ms
+
+        self.hs.clock.now = 5000  # seconds
+        self.hs.config.expire_access_token = True
+
+        user_info = yield self.auth.get_user_from_macaroon(macaroon.serialize())
+        user = user_info["user"]
+        self.assertEqual(UserID.from_string(user_id), user)
diff --git a/tests/handlers/test_register.py b/tests/handlers/test_register.py
index 69a5e5b1d..a7de3c7c1 100644
--- a/tests/handlers/test_register.py
+++ b/tests/handlers/test_register.py
@@ -42,12 +42,12 @@ class RegistrationTestCase(unittest.TestCase):
             http_client=None,
             expire_access_token=True)
         self.auth_handler = Mock(
-            generate_short_term_login_token=Mock(return_value='secret'))
+            generate_access_token=Mock(return_value='secret'))
         self.hs.handlers = RegistrationHandlers(self.hs)
         self.handler = self.hs.get_handlers().registration_handler
         self.hs.get_handlers().profile_handler = Mock()
         self.mock_handler = Mock(spec=[
-            "generate_short_term_login_token",
+            "generate_access_token",
         ])
         self.hs.get_auth_handler = Mock(return_value=self.auth_handler)