diff --git a/changelog.d/7999.bugfix b/changelog.d/7999.bugfix
new file mode 100644
index 0000000000..e0b8c4922f
--- /dev/null
+++ b/changelog.d/7999.bugfix
@@ -0,0 +1 @@
+Fix a long standing bug where HTTP HEAD requests resulted in a 400 error.
diff --git a/synapse/http/server.py b/synapse/http/server.py
index d4f9ad6e67..94ab29974a 100644
--- a/synapse/http/server.py
+++ b/synapse/http/server.py
@@ -242,10 +242,12 @@ class _AsyncResource(resource.Resource, metaclass=abc.ABCMeta):
         no appropriate method exists. Can be overriden in sub classes for
         different routing.
         """
+        # Treat HEAD requests as GET requests.
+        request_method = request.method.decode("ascii")
+        if request_method == "HEAD":
+            request_method = "GET"
 
-        method_handler = getattr(
-            self, "_async_render_%s" % (request.method.decode("ascii"),), None
-        )
+        method_handler = getattr(self, "_async_render_%s" % (request_method,), None)
         if method_handler:
             raw_callback_return = method_handler(request)
 
@@ -362,11 +364,15 @@ class JsonResource(DirectServeJsonResource):
             A tuple of the callback to use, the name of the servlet, and the
             key word arguments to pass to the callback
         """
+        # Treat HEAD requests as GET requests.
         request_path = request.path.decode("ascii")
+        request_method = request.method
+        if request_method == b"HEAD":
+            request_method = b"GET"
 
         # Loop through all the registered callbacks to check if the method
         # and path regex match
-        for path_entry in self.path_regexs.get(request.method, []):
+        for path_entry in self.path_regexs.get(request_method, []):
             m = path_entry.pattern.match(request_path)
             if m:
                 # We found a match!
@@ -579,7 +585,7 @@ def set_cors_headers(request: Request):
     """
     request.setHeader(b"Access-Control-Allow-Origin", b"*")
     request.setHeader(
-        b"Access-Control-Allow-Methods", b"GET, POST, PUT, DELETE, OPTIONS"
+        b"Access-Control-Allow-Methods", b"GET, HEAD, POST, PUT, DELETE, OPTIONS"
     )
     request.setHeader(
         b"Access-Control-Allow-Headers",
diff --git a/tests/test_server.py b/tests/test_server.py
index 073b2362cc..d628070e48 100644
--- a/tests/test_server.py
+++ b/tests/test_server.py
@@ -157,6 +157,29 @@ class JsonResourceTests(unittest.TestCase):
         self.assertEqual(channel.json_body["error"], "Unrecognized request")
         self.assertEqual(channel.json_body["errcode"], "M_UNRECOGNIZED")
 
+    def test_head_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.
+        """
+
+        def _callback(request, **kwargs):
+            return 200, {"result": True}
+
+        res = JsonResource(self.homeserver)
+        res.register_paths(
+            "GET", [re.compile("^/_matrix/foo$")], _callback, "test_servlet",
+        )
+
+        # The path was registered as GET, but this is a HEAD request.
+        request, channel = make_request(self.reactor, b"HEAD", b"/_matrix/foo")
+        render(request, res, self.reactor)
+
+        self.assertEqual(channel.result["code"], b"200")
+        self.assertNotIn("body", channel.result)
+        self.assertEqual(channel.headers.getRawHeaders(b"Content-Length"), [b"15"])
+
 
 class OptionsResourceTests(unittest.TestCase):
     def setUp(self):
@@ -255,7 +278,7 @@ class WrapHtmlRequestHandlerTests(unittest.TestCase):
         self.reactor = ThreadedMemoryReactorClock()
 
     def test_good_response(self):
-        def callback(request):
+        async def callback(request):
             request.write(b"response")
             request.finish()
 
@@ -275,7 +298,7 @@ class WrapHtmlRequestHandlerTests(unittest.TestCase):
         with the right location.
         """
 
-        def callback(request, **kwargs):
+        async def callback(request, **kwargs):
             raise RedirectException(b"/look/an/eagle", 301)
 
         res = WrapHtmlRequestHandlerTests.TestResource()
@@ -295,7 +318,7 @@ class WrapHtmlRequestHandlerTests(unittest.TestCase):
         returned too
         """
 
-        def callback(request, **kwargs):
+        async def callback(request, **kwargs):
             e = RedirectException(b"/no/over/there", 304)
             e.cookies.append(b"session=yespls")
             raise e
@@ -312,3 +335,19 @@ class WrapHtmlRequestHandlerTests(unittest.TestCase):
         self.assertEqual(location_headers, [b"/no/over/there"])
         cookies_headers = [v for k, v in headers if k == b"Set-Cookie"]
         self.assertEqual(cookies_headers, [b"session=yespls"])
+
+    def test_head_request(self):
+        """A head request should work by being turned into a GET request."""
+
+        async def callback(request):
+            request.write(b"response")
+            request.finish()
+
+        res = WrapHtmlRequestHandlerTests.TestResource()
+        res.callback = callback
+
+        request, channel = make_request(self.reactor, b"HEAD", b"/path")
+        render(request, res, self.reactor)
+
+        self.assertEqual(channel.result["code"], b"200")
+        self.assertNotIn("body", channel.result)