diff --git a/.circleci/config.yml b/.circleci/config.yml
index 5266544f3c37..605430fb3f09 100644
--- a/.circleci/config.yml
+++ b/.circleci/config.yml
@@ -53,7 +53,7 @@ jobs:
     steps:
       - checkout
       - run: docker pull matrixdotorg/sytest-synapsepy3
-      - run: docker run --rm -it -v $(pwd)\:/src -v $(pwd)/logs\:/logs hawkowl/sytestpy3
+      - run: docker run --rm -it -v $(pwd)\:/src -v $(pwd)/logs\:/logs matrixdotorg/sytest-synapsepy3
       - store_artifacts:
           path: ~/project/logs
           destination: logs
@@ -76,7 +76,7 @@ jobs:
       - checkout
       - run: bash .circleci/merge_base_branch.sh
       - run: docker pull matrixdotorg/sytest-synapsepy3
-      - run: docker run --rm -it -v $(pwd)\:/src -v $(pwd)/logs\:/logs hawkowl/sytestpy3
+      - run: docker run --rm -it -v $(pwd)\:/src -v $(pwd)/logs\:/logs matrixdotorg/sytest-synapsepy3
       - store_artifacts:
           path: ~/project/logs
           destination: logs
@@ -101,6 +101,8 @@ workflows:
     jobs:
       - sytestpy2
       - sytestpy2postgres
+      - sytestpy3
+      - sytestpy3postgres
       - sytestpy2merged:
           filters:
             branches:
@@ -109,6 +111,11 @@ workflows:
           filters:
             branches:
               ignore: /develop|master/
-# Currently broken while the Python 3 port is incomplete
-#      - sytestpy3
-#      - sytestpy3postgres
+      - sytestpy3merged:
+          filters:
+            branches:
+              ignore: /develop|master/
+      - sytestpy3postgresmerged:
+          filters:
+            branches:
+              ignore: /develop|master/
diff --git a/.travis.yml b/.travis.yml
index ebc972ed2492..b3ee66da8ff1 100644
--- a/.travis.yml
+++ b/.travis.yml
@@ -25,6 +25,9 @@ matrix:
     services:
       - postgresql
 
+  - python: 3.5
+    env: TOX_ENV=py35
+
   - python: 3.6
     env: TOX_ENV=py36
 
diff --git a/changelog.d/3576.feature b/changelog.d/3576.feature
new file mode 100644
index 000000000000..02a10e370da2
--- /dev/null
+++ b/changelog.d/3576.feature
@@ -0,0 +1 @@
+Python 3.5+ is now supported.
diff --git a/synapse/http/client.py b/synapse/http/client.py
index 4ba54fed05ef..d60f87b04ea0 100644
--- a/synapse/http/client.py
+++ b/synapse/http/client.py
@@ -348,7 +348,8 @@ def get_file(self, url, output_stream, max_size=None, headers=None):
 
         resp_headers = dict(response.headers.getAllRawHeaders())
 
-        if 'Content-Length' in resp_headers and resp_headers['Content-Length'] > max_size:
+        if (b'Content-Length' in resp_headers and
+                int(resp_headers[b'Content-Length']) > max_size):
             logger.warn("Requested URL is too large > %r bytes" % (self.max_size,))
             raise SynapseError(
                 502,
@@ -381,7 +382,12 @@ def get_file(self, url, output_stream, max_size=None, headers=None):
             )
 
         defer.returnValue(
-            (length, resp_headers, response.request.absoluteURI, response.code),
+            (
+                length,
+                resp_headers,
+                response.request.absoluteURI.decode('ascii'),
+                response.code,
+            ),
         )
 
 
@@ -466,9 +472,9 @@ def __init__(self, hs):
     def endpointForURI(self, uri):
         logger.info("Getting endpoint for %s", uri.toBytes())
 
-        if uri.scheme == "http":
+        if uri.scheme == b"http":
             endpoint_factory = HostnameEndpoint
-        elif uri.scheme == "https":
+        elif uri.scheme == b"https":
             tlsCreator = self.policyForHTTPS.creatorForNetloc(uri.host, uri.port)
 
             def endpoint_factory(reactor, host, port, **kw):
diff --git a/synapse/push/httppusher.py b/synapse/push/httppusher.py
index 81e18bcf7d98..48abd5e4d689 100644
--- a/synapse/push/httppusher.py
+++ b/synapse/push/httppusher.py
@@ -15,6 +15,8 @@
 # limitations under the License.
 import logging
 
+import six
+
 from prometheus_client import Counter
 
 from twisted.internet import defer
@@ -26,6 +28,9 @@
 
 from . import push_rule_evaluator, push_tools
 
+if six.PY3:
+    long = int
+
 logger = logging.getLogger(__name__)
 
 http_push_processed_counter = Counter("synapse_http_httppusher_http_pushes_processed", "")
@@ -96,7 +101,7 @@ def on_started(self):
 
     @defer.inlineCallbacks
     def on_new_notifications(self, min_stream_ordering, max_stream_ordering):
-        self.max_stream_ordering = max(max_stream_ordering, self.max_stream_ordering)
+        self.max_stream_ordering = max(max_stream_ordering, self.max_stream_ordering or 0)
         yield self._process()
 
     @defer.inlineCallbacks
diff --git a/synapse/push/mailer.py b/synapse/push/mailer.py
index bfa6df7b68b8..b78ce10396b7 100644
--- a/synapse/push/mailer.py
+++ b/synapse/push/mailer.py
@@ -17,10 +17,11 @@
 import email.utils
 import logging
 import time
-import urllib
 from email.mime.multipart import MIMEMultipart
 from email.mime.text import MIMEText
 
+from six.moves import urllib
+
 import bleach
 import jinja2
 
@@ -474,7 +475,7 @@ def make_unsubscribe_link(self, user_id, app_id, email_address):
         # XXX: make r0 once API is stable
         return "%s_matrix/client/unstable/pushers/remove?%s" % (
             self.hs.config.public_baseurl,
-            urllib.urlencode(params),
+            urllib.parse.urlencode(params),
         )
 
 
@@ -561,7 +562,7 @@ def mxc_to_http_filter(value, width, height, resize_method="crop"):
         return "%s_matrix/media/v1/thumbnail/%s?%s%s" % (
             config.public_baseurl,
             serverAndMediaId,
-            urllib.urlencode(params),
+            urllib.parse.urlencode(params),
             fragment or "",
         )
 
diff --git a/synapse/replication/slave/storage/devices.py b/synapse/replication/slave/storage/devices.py
index 8206a988f793..21b8c468facd 100644
--- a/synapse/replication/slave/storage/devices.py
+++ b/synapse/replication/slave/storage/devices.py
@@ -13,6 +13,8 @@
 # See the License for the specific language governing permissions and
 # limitations under the License.
 
+import six
+
 from synapse.storage import DataStore
 from synapse.storage.end_to_end_keys import EndToEndKeyStore
 from synapse.util.caches.stream_change_cache import StreamChangeCache
@@ -21,6 +23,13 @@
 from ._slaved_id_tracker import SlavedIdTracker
 
 
+def __func__(inp):
+    if six.PY3:
+        return inp
+    else:
+        return inp.__func__
+
+
 class SlavedDeviceStore(BaseSlavedStore):
     def __init__(self, db_conn, hs):
         super(SlavedDeviceStore, self).__init__(db_conn, hs)
@@ -38,14 +47,14 @@ def __init__(self, db_conn, hs):
             "DeviceListFederationStreamChangeCache", device_list_max,
         )
 
-    get_device_stream_token = DataStore.get_device_stream_token.__func__
-    get_user_whose_devices_changed = DataStore.get_user_whose_devices_changed.__func__
-    get_devices_by_remote = DataStore.get_devices_by_remote.__func__
-    _get_devices_by_remote_txn = DataStore._get_devices_by_remote_txn.__func__
-    _get_e2e_device_keys_txn = DataStore._get_e2e_device_keys_txn.__func__
-    mark_as_sent_devices_by_remote = DataStore.mark_as_sent_devices_by_remote.__func__
+    get_device_stream_token = __func__(DataStore.get_device_stream_token)
+    get_user_whose_devices_changed = __func__(DataStore.get_user_whose_devices_changed)
+    get_devices_by_remote = __func__(DataStore.get_devices_by_remote)
+    _get_devices_by_remote_txn = __func__(DataStore._get_devices_by_remote_txn)
+    _get_e2e_device_keys_txn = __func__(DataStore._get_e2e_device_keys_txn)
+    mark_as_sent_devices_by_remote = __func__(DataStore.mark_as_sent_devices_by_remote)
     _mark_as_sent_devices_by_remote_txn = (
-        DataStore._mark_as_sent_devices_by_remote_txn.__func__
+        __func__(DataStore._mark_as_sent_devices_by_remote_txn)
     )
     count_e2e_one_time_keys = EndToEndKeyStore.__dict__["count_e2e_one_time_keys"]
 
diff --git a/tox.ini b/tox.ini
index 085f43898908..80ac9324df76 100644
--- a/tox.ini
+++ b/tox.ini
@@ -64,49 +64,11 @@ setenv =
     {[base]setenv}
     SYNAPSE_POSTGRES = 1
 
+[testenv:py35]
+usedevelop=true
+
 [testenv:py36]
 usedevelop=true
-commands =
-    /usr/bin/find "{toxinidir}" -name '*.pyc' -delete
-    coverage run {env:COVERAGE_OPTS:} --source="{toxinidir}/synapse" \
-        "{envbindir}/trial" {env:TRIAL_FLAGS:} {posargs:tests/config \
-		tests/api/test_filtering.py \
-		tests/api/test_ratelimiting.py \
-		tests/appservice \
-		tests/crypto \
-		tests/events \
-		tests/handlers/test_appservice.py \
-		tests/handlers/test_auth.py \
-		tests/handlers/test_device.py \
-		tests/handlers/test_directory.py \
-		tests/handlers/test_e2e_keys.py \
-		tests/handlers/test_presence.py \
-		tests/handlers/test_profile.py \
-		tests/handlers/test_register.py \
-		tests/replication/slave/storage/test_account_data.py \
-		tests/replication/slave/storage/test_receipts.py \
-		tests/storage/test_appservice.py \
-		tests/storage/test_background_update.py \
-		tests/storage/test_base.py \
-		tests/storage/test__base.py \
-		tests/storage/test_client_ips.py \
-		tests/storage/test_devices.py \
-		tests/storage/test_end_to_end_keys.py \
-		tests/storage/test_event_push_actions.py \
-		tests/storage/test_keys.py \
-		tests/storage/test_presence.py \
-		tests/storage/test_profile.py \
-		tests/storage/test_registration.py \
-		tests/storage/test_room.py \
-		tests/storage/test_user_directory.py \
-		tests/test_distributor.py \
-		tests/test_dns.py \
-		tests/test_preview.py \
-		tests/test_test_utils.py \
-		tests/test_types.py \
-		tests/util} \
-        {env:TOXSUFFIX:}
-    {env:DUMP_COVERAGE_COMMAND:coverage report -m}
 
 [testenv:packaging]
 deps =