diff --git a/changelog.d/3446.misc b/changelog.d/3446.misc
new file mode 100644
index 000000000..e69de29bb
diff --git a/tests/server.py b/tests/server.py
new file mode 100644
index 000000000..73069dff5
--- /dev/null
+++ b/tests/server.py
@@ -0,0 +1,181 @@
+from io import BytesIO
+
+import attr
+import json
+from six import text_type
+
+from twisted.python.failure import Failure
+from twisted.internet.defer import Deferred
+from twisted.test.proto_helpers import MemoryReactorClock
+
+from synapse.http.site import SynapseRequest
+from twisted.internet import threads
+from tests.utils import setup_test_homeserver as _sth
+
+
+@attr.s
+class FakeChannel(object):
+    """
+    A fake Twisted Web Channel (the part that interfaces with the
+    wire).
+    """
+
+    result = attr.ib(factory=dict)
+
+    @property
+    def json_body(self):
+        if not self.result:
+            raise Exception("No result yet.")
+        return json.loads(self.result["body"])
+
+    def writeHeaders(self, version, code, reason, headers):
+        self.result["version"] = version
+        self.result["code"] = code
+        self.result["reason"] = reason
+        self.result["headers"] = headers
+
+    def write(self, content):
+        if "body" not in self.result:
+            self.result["body"] = b""
+
+        self.result["body"] += content
+
+    def requestDone(self, _self):
+        self.result["done"] = True
+
+    def getPeer(self):
+        return None
+
+    def getHost(self):
+        return None
+
+    @property
+    def transport(self):
+        return self
+
+
+class FakeSite:
+    """
+    A fake Twisted Web Site, with mocks of the extra things that
+    Synapse adds.
+    """
+
+    server_version_string = b"1"
+    site_tag = "test"
+
+    @property
+    def access_logger(self):
+        class FakeLogger:
+            def info(self, *args, **kwargs):
+                pass
+
+        return FakeLogger()
+
+
+def make_request(method, path, content=b""):
+    """
+    Make a web request using the given method and path, feed it the
+    content, and return the Request and the Channel underneath.
+    """
+
+    if isinstance(content, text_type):
+        content = content.encode('utf8')
+
+    site = FakeSite()
+    channel = FakeChannel()
+
+    req = SynapseRequest(site, channel)
+    req.process = lambda: b""
+    req.content = BytesIO(content)
+    req.requestReceived(method, path, b"1.1")
+
+    return req, channel
+
+
+def wait_until_result(clock, channel, timeout=100):
+    """
+    Wait until the channel has a result.
+    """
+    clock.run()
+    x = 0
+
+    while not channel.result:
+        x += 1
+
+        if x > timeout:
+            raise Exception("Timed out waiting for request to finish.")
+
+        clock.advance(0.1)
+
+
+class ThreadedMemoryReactorClock(MemoryReactorClock):
+    """
+    A MemoryReactorClock that supports callFromThread.
+    """
+    def callFromThread(self, callback, *args, **kwargs):
+        """
+        Make the callback fire in the next reactor iteration.
+        """
+        d = Deferred()
+        d.addCallback(lambda x: callback(*args, **kwargs))
+        self.callLater(0, d.callback, True)
+        return d
+
+
+def setup_test_homeserver(*args, **kwargs):
+    """
+    Set up a synchronous test server, driven by the reactor used by
+    the homeserver.
+    """
+    d = _sth(*args, **kwargs).result
+
+    # Make the thread pool synchronous.
+    clock = d.get_clock()
+    pool = d.get_db_pool()
+
+    def runWithConnection(func, *args, **kwargs):
+        return threads.deferToThreadPool(
+            pool._reactor,
+            pool.threadpool,
+            pool._runWithConnection,
+            func,
+            *args,
+            **kwargs
+        )
+
+    def runInteraction(interaction, *args, **kwargs):
+        return threads.deferToThreadPool(
+            pool._reactor,
+            pool.threadpool,
+            pool._runInteraction,
+            interaction,
+            *args,
+            **kwargs
+        )
+
+    pool.runWithConnection = runWithConnection
+    pool.runInteraction = runInteraction
+
+    class ThreadPool:
+        """
+        Threadless thread pool.
+        """
+        def start(self):
+            pass
+
+        def callInThreadWithCallback(self, onResult, function, *args, **kwargs):
+            def _(res):
+                if isinstance(res, Failure):
+                    onResult(False, res)
+                else:
+                    onResult(True, res)
+
+            d = Deferred()
+            d.addCallback(lambda x: function(*args, **kwargs))
+            d.addBoth(_)
+            clock._reactor.callLater(0, d.callback, True)
+            return d
+
+    clock.threadpool = ThreadPool()
+    pool.threadpool = ThreadPool()
+    return d
diff --git a/tests/test_server.py b/tests/test_server.py
new file mode 100644
index 000000000..8ad822c43
--- /dev/null
+++ b/tests/test_server.py
@@ -0,0 +1,128 @@
+import json
+import re
+
+from twisted.internet.defer import Deferred
+from twisted.test.proto_helpers import MemoryReactorClock
+
+from synapse.util import Clock
+from synapse.api.errors import Codes, SynapseError
+from synapse.http.server import JsonResource
+from tests import unittest
+from tests.server import make_request, setup_test_homeserver
+
+
+class JsonResourceTests(unittest.TestCase):
+    def setUp(self):
+        self.reactor = MemoryReactorClock()
+        self.hs_clock = Clock(self.reactor)
+        self.homeserver = setup_test_homeserver(
+            http_client=None, clock=self.hs_clock, reactor=self.reactor
+        )
+
+    def test_handler_for_request(self):
+        """
+        JsonResource.handler_for_request gives correctly decoded URL args to
+        the callback, while Twisted will give the raw bytes of URL query
+        arguments.
+        """
+        got_kwargs = {}
+
+        def _callback(request, **kwargs):
+            got_kwargs.update(kwargs)
+            return (200, kwargs)
+
+        res = JsonResource(self.homeserver)
+        res.register_paths("GET", [re.compile("^/foo/(?P<room_id>[^/]*)$")], _callback)
+
+        request, channel = make_request(b"GET", b"/foo/%E2%98%83?a=%E2%98%83")
+        request.render(res)
+
+        self.assertEqual(request.args, {b'a': [u"\N{SNOWMAN}".encode('utf8')]})
+        self.assertEqual(got_kwargs, {u"room_id": u"\N{SNOWMAN}"})
+
+    def test_callback_direct_exception(self):
+        """
+        If the web callback raises an uncaught exception, it will be translated
+        into a 500.
+        """
+
+        def _callback(request, **kwargs):
+            raise Exception("boo")
+
+        res = JsonResource(self.homeserver)
+        res.register_paths("GET", [re.compile("^/foo$")], _callback)
+
+        request, channel = make_request(b"GET", b"/foo")
+        request.render(res)
+
+        self.assertEqual(channel.result["code"], b'500')
+
+    def test_callback_indirect_exception(self):
+        """
+        If the web callback raises an uncaught exception in a Deferred, it will
+        be translated into a 500.
+        """
+
+        def _throw(*args):
+            raise Exception("boo")
+
+        def _callback(request, **kwargs):
+            d = Deferred()
+            d.addCallback(_throw)
+            self.reactor.callLater(1, d.callback, True)
+            return d
+
+        res = JsonResource(self.homeserver)
+        res.register_paths("GET", [re.compile("^/foo$")], _callback)
+
+        request, channel = make_request(b"GET", b"/foo")
+        request.render(res)
+
+        # No error has been raised yet
+        self.assertTrue("code" not in channel.result)
+
+        # Advance time, now there's an error
+        self.reactor.advance(1)
+        self.assertEqual(channel.result["code"], b'500')
+
+    def test_callback_synapseerror(self):
+        """
+        If the web callback raises a SynapseError, it returns the appropriate
+        status code and message set in it.
+        """
+
+        def _callback(request, **kwargs):
+            raise SynapseError(403, "Forbidden!!one!", Codes.FORBIDDEN)
+
+        res = JsonResource(self.homeserver)
+        res.register_paths("GET", [re.compile("^/foo$")], _callback)
+
+        request, channel = make_request(b"GET", b"/foo")
+        request.render(res)
+
+        self.assertEqual(channel.result["code"], b'403')
+        reply_body = json.loads(channel.result["body"])
+        self.assertEqual(reply_body["error"], "Forbidden!!one!")
+        self.assertEqual(reply_body["errcode"], "M_FORBIDDEN")
+
+    def test_no_handler(self):
+        """
+        If there is no handler to process the request, Synapse will return 400.
+        """
+
+        def _callback(request, **kwargs):
+            """
+            Not ever actually called!
+            """
+            self.fail("shouldn't ever get here")
+
+        res = JsonResource(self.homeserver)
+        res.register_paths("GET", [re.compile("^/foo$")], _callback)
+
+        request, channel = make_request(b"GET", b"/foobar")
+        request.render(res)
+
+        self.assertEqual(channel.result["code"], b'400')
+        reply_body = json.loads(channel.result["body"])
+        self.assertEqual(reply_body["error"], "Unrecognized request")
+        self.assertEqual(reply_body["errcode"], "M_UNRECOGNIZED")