diff --git a/changelog.d/19879.misc b/changelog.d/19879.misc
new file mode 100644
index 00000000000..be10ee05403
--- /dev/null
+++ b/changelog.d/19879.misc
@@ -0,0 +1 @@
+Update `HomeserverTestCase.get_success(...)` and friends to drive async Rust (Tokio runtime/thread pool).
diff --git a/tests/rest/client/sliding_sync/test_sliding_sync.py b/tests/rest/client/sliding_sync/test_sliding_sync.py
index 2fd18f0e545..c43ed650174 100644
--- a/tests/rest/client/sliding_sync/test_sliding_sync.py
+++ b/tests/rest/client/sliding_sync/test_sliding_sync.py
@@ -566,7 +566,9 @@ def test_wait_for_sync_token(self) -> None:
         # timeout
         with self.assertRaises(TimedOutException):
             channel.await_result(timeout_ms=9900)
-        channel.await_result(timeout_ms=200)
+        # `notifier.wait_for_stream_token(from_token)` only checks every 500ms so we
+        # need to match that in order to make sure we hit the wake-up for sure.
+        channel.await_result(timeout_ms=500)
         self.assertEqual(channel.code, 200, channel.json_body)
 
         # We expect the next `pos` in the result to be the same as what we requested
diff --git a/tests/server.py b/tests/server.py
index eea11b301f9..a8e5d655652 100644
--- a/tests/server.py
+++ b/tests/server.py
@@ -101,6 +101,7 @@
 from synapse.storage.prepare_database import prepare_database
 from synapse.types import ISynapseReactor, JsonDict
 from synapse.util.clock import Clock
+from synapse.util.duration import Duration
 from synapse.util.json import json_encoder
 
 from tests.utils import (
@@ -301,15 +302,85 @@ def transport(self) -> "FakeChannel":
     def await_result(self, timeout_ms: int = 1000) -> None:
         """
         Wait until the request is finished.
+
+        Advances the Twisted reactor clock by 0.1s and suspending execution of the
+        Python thread (to allow other threads to do work) in a loop until we see a
+        result. We timeout when both the Twisted reactor clock has been advanced enough
+        AND we've waited the 1s of real-time before giving up.
+
+        The loop 1) allows `clock.call_later` scheduled callbacks to run if they are
+        scheduled to run now and 2) will also allow other threads to make progress. This
+        could be things spawned on the Twisted reactor threadpool or Tokio runtime
+        (async Rust code).
+
+        Args:
+            timeout_ms: The Twisted reactor time we wait until we raise a `TimedOutException`
         """
-        end_time = self._reactor.seconds() + timeout_ms / 1000.0
+        timeout = Duration(milliseconds=timeout_ms)
+        start_time_seconds = self._reactor.seconds()
+
+        # 1s is an arbitrary small number so we don't have to wait that long when
+        # something is stuck and because we assume any task on another thread will be
+        # fast enough.
+        #
+        # We don't use the same `timeout_ms` passed in because some tests specify 20s
+        # and we don't want to be waiting that long unnecessarily.
+        real_time_timeout = Duration(seconds=1)
+        start_real_time_seconds = time.time()
+
+        # TODO: Why?
         self._reactor.run()
 
+        loop_count = 0
         while not self.is_finished():
-            if self._reactor.seconds() > end_time:
+            if (
+                # Exceeded the Twisted reactor time timeout
+                #
+                # We use `>=` for the reactor time condition as it's possible we advance
+                # exactly the `timeout` amount and we don't want to get stuck in an
+                # infinite loop
+                self._reactor.seconds() >= start_time_seconds + timeout.as_secs()
+                # And exceeded the real-time timeout
+                and time.time() > start_real_time_seconds + real_time_timeout.as_secs()
+            ):
                 raise TimedOutException("Timed out waiting for request to finish.")
 
-            self._reactor.advance(0.1)
+            # Suspend execution of this thread to allow other threads to do work. This
+            # could be things spawned on the Twisted reactor threadpool or Tokio thread
+            # pool (async Rust code).
+            #
+            # Note: Since we're waiting real-time (`timeout` duration), the tests also
+            # pass with `time.sleep(0)` commented out because Python has a default
+            # thread switch interval (5ms for cpython) (see
+            # `sys.setswitchinterval(interval)`). We still want this here as we're able
+            # to preempt and cause the thread context swtich to happen faster.
+            #
+            # After a few cycles, we use `time.sleep(0.001)` instead of `time.sleep(0)`
+            # to avoid tightlooping on the main thread (CPU 100%) because it's wasteful
+            # and may starve out other threads. 10 is arbitrary but many cases will have
+            # none or only a few round-trips so we can just try to go as fast as
+            # posssible.
+            if loop_count < 10:
+                time.sleep(0)
+            else:
+                time.sleep(0.001)
+
+            # Advance the Twisted reactor and run any scheduled callbacks
+            #
+            # Don't advance the Twisted reactor clock further than the timeout duration
+            # as someone should increase the timeout if they expect things to take
+            # longer.
+            if self._reactor.seconds() < start_time_seconds + timeout.as_secs():
+                self._reactor.advance(0.1)
+            else:
+                # But we want to still keep running whatever might be getting scheduled
+                # to run now.
+                #
+                # For example from other threads, they may have scheduled something on
+                # the reactor to run (like `reactor.callFromThread(...)`)
+                self._reactor.advance(0)
+
+            loop_count += 1
 
     def extract_cookies(self, cookies: MutableMapping[str, str]) -> None:
         """Process the contents of any Set-Cookie headers in the response