diff --git a/pytest_httpserver/httpserver.py b/pytest_httpserver/httpserver.py
index 5513c0b..c28a4e0 100644
--- a/pytest_httpserver/httpserver.py
+++ b/pytest_httpserver/httpserver.py
@@ -1073,6 +1073,8 @@ def __init__(
             self.default_waiting_settings = WaitingSettings()
         self._waiting_settings = copy(self.default_waiting_settings)
         self._waiting_result: queue.LifoQueue[bool] = queue.LifoQueue(maxsize=1)
+        self._handler_lock = threading.RLock()
+        self._active_waiting_handlers = 0
         self.startup_timeout = startup_timeout
         self._readiness_check_pending = False
 
@@ -1422,27 +1424,31 @@ def dispatch(self, request: Request) -> Response:
         if self.permanently_failed:
             return self.respond_permanent_failure()
 
-        handler = None
-        if self.ordered_handlers:
-            handler = self.ordered_handlers[0]
-            if not handler.matcher.match(request):
-                self.permanently_failed = True
-                response = self.respond_nohandler(request)
-                return response
-
-            self.ordered_handlers.pop(0)
-            self._update_waiting_result()
-
-        if not handler:
-            handler = self.oneshot_handlers.match(request)
-            if handler:
-                self.oneshot_handlers.remove(handler)
-                self._update_waiting_result()
-            else:
-                handler = self.handlers.match(request)
+        with self._handler_lock:
+            handler = None
+            consumed_handler = False
+            if self.ordered_handlers:
+                handler = self.ordered_handlers[0]
+                if not handler.matcher.match(request):
+                    self.permanently_failed = True
+                    response = self.respond_nohandler(request)
+                    return response
+
+                self.ordered_handlers.pop(0)
+                consumed_handler = True
 
             if not handler:
-                return self.respond_nohandler(request)
+                handler = self.oneshot_handlers.match(request)
+                if handler:
+                    self.oneshot_handlers.remove(handler)
+                    consumed_handler = True
+                else:
+                    handler = self.handlers.match(request)
+
+                if not handler:
+                    return self.respond_nohandler(request)
+            if consumed_handler:
+                self._active_waiting_handlers += 1
 
         try:
             response = handler.respond(request)
@@ -1455,6 +1461,11 @@ def dispatch(self, request: Request) -> Response:
         except Exception as e:
             self.handler_errors.append(e)
             raise
+        finally:
+            if consumed_handler:
+                with self._handler_lock:
+                    self._active_waiting_handlers -= 1
+                    self._update_waiting_result()
 
         if response is None:
             response = Response("")
@@ -1473,7 +1484,7 @@ def _set_waiting_result(self, value: bool) -> None:  # noqa: FBT001
             self._waiting_result.put_nowait(value)
 
     def _update_waiting_result(self) -> None:
-        if not self.oneshot_handlers and not self.ordered_handlers:
+        if not self.oneshot_handlers and not self.ordered_handlers and not self._active_waiting_handlers:
             self._set_waiting_result(value=True)
 
     @contextmanager
diff --git a/releasenotes/notes/wait-handler-completion-0a17b0e62fbb76a1.yaml b/releasenotes/notes/wait-handler-completion-0a17b0e62fbb76a1.yaml
new file mode 100644
index 0000000..4b9f605
--- /dev/null
+++ b/releasenotes/notes/wait-handler-completion-0a17b0e62fbb76a1.yaml
@@ -0,0 +1,5 @@
+fixes:
+  - |
+    Wait for ordered and oneshot response callbacks to finish before reporting
+    successful completion from ``HTTPServer.wait()``, including callbacks
+    executing concurrently in a threaded server.
diff --git a/tests/test_wait.py b/tests/test_wait.py
index d23f65d..145a287 100644
--- a/tests/test_wait.py
+++ b/tests/test_wait.py
@@ -1,6 +1,13 @@
+from contextlib import closing
+from http.client import HTTPConnection
+from threading import Event
+
 import requests
 from pytest import approx
+from pytest import mark
 from pytest import raises
+from werkzeug import Request
+from werkzeug import Response
 
 from pytest_httpserver import HTTPServer
 
@@ -70,3 +77,63 @@ def test_wait_raise_assertion_false(httpserver: HTTPServer):
     assert not waiting.result
     waiting_time_error = 0.1
     assert waiting.elapsed_time == approx(waiting_timeout, abs=waiting_time_error)
+
+
+@mark.parametrize("ordered", [False, True])
+def test_wait_does_not_finish_while_last_handler_is_running(httpserver: HTTPServer, *, ordered: bool):
+    entered = Event()
+    release = Event()
+
+    def respond(_request: Request) -> Response:
+        entered.set()
+        assert release.wait(5)
+        return Response("finished")
+
+    handler = httpserver.expect_ordered_request("/") if ordered else httpserver.expect_oneshot_request("/")
+    handler.respond_with_handler(respond)
+    with closing(HTTPConnection(httpserver.host, httpserver.port, timeout=5)) as connection:
+        try:
+            with httpserver.wait(timeout=0.01, raise_assertions=False) as waiting:
+                connection.request("GET", "/")
+                assert entered.wait(5)
+            assert not waiting.result
+        finally:
+            release.set()
+            assert connection.getresponse().read() == b"finished"
+
+
+@mark.parametrize("ordered", [False, True])
+def test_wait_tracks_other_callbacks_after_handler_lists_are_empty(*, ordered: bool):
+    entered = [Event(), Event()]
+    release = [Event(), Event()]
+
+    def respond(request: Request) -> Response:
+        index = int(request.path[1:])
+        entered[index].set()
+        assert release[index].wait(5)
+        return Response("finished")
+
+    with HTTPServer(threaded=True) as server:
+        for index in range(2):
+            handler = (
+                server.expect_ordered_request(f"/{index}") if ordered else server.expect_oneshot_request(f"/{index}")
+            )
+            handler.respond_with_handler(respond)
+
+        with (
+            closing(HTTPConnection(server.host, server.port, timeout=5)) as first,
+            closing(HTTPConnection(server.host, server.port, timeout=5)) as second,
+        ):
+            try:
+                with server.wait(timeout=0.01, raise_assertions=False) as waiting:
+                    first.request("GET", "/0")
+                    assert entered[0].wait(5)
+                    second.request("GET", "/1")
+                    assert entered[1].wait(5)
+                    release[1].set()
+                    assert second.getresponse().read() == b"finished"
+                assert not waiting.result
+            finally:
+                release[0].set()
+                release[1].set()
+                assert first.getresponse().read() == b"finished"