diff --git a/CHANGES.rst b/CHANGES.rst
index 1dbb9605..f7508afd 100644
--- a/CHANGES.rst
+++ b/CHANGES.rst
@@ -61,6 +61,9 @@ Unreleased
 -   Blueprints have a ``cli`` Click group like ``app.cli``. CLI commands
     registered with a blueprint will be available as a group under the
     ``flask`` command. :issue:`1357`.
+-   When using the test client as a context manager (``with client:``),
+    all preserved request contexts are popped when the block exits,
+    ensuring nested contexts are cleaned up correctly. :pr:`3157`
 
 .. _#2935: https://github.com/pallets/flask/issues/2935
 .. _#2957: https://github.com/pallets/flask/issues/2957
diff --git a/flask/testing.py b/flask/testing.py
index 6c9de313..f2fbad6c 100644
--- a/flask/testing.py
+++ b/flask/testing.py
@@ -206,12 +206,17 @@ class FlaskClient(Client):
     def __exit__(self, exc_type, exc_value, tb):
         self.preserve_context = False
 
-        # on exit we want to clean up earlier.  Normally the request context
-        # stays preserved until the next request in the same thread comes
-        # in.  See RequestGlobals.push() for the general behavior.
-        top = _request_ctx_stack.top
-        if top is not None and top.preserved:
-            top.pop()
+        # Normally the request context is preserved until the next
+        # request in the same thread comes. When the client exits we
+        # want to clean up earlier. Pop request contexts until the stack
+        # is empty or a non-preserved one is found.
+        while True:
+            top = _request_ctx_stack.top
+
+            if top is not None and top.preserved:
+                top.pop()
+            else:
+                break
 
 
 class FlaskCliRunner(CliRunner):
diff --git a/tests/test_testing.py b/tests/test_testing.py
index a6b9d70e..ae0f54d9 100644
--- a/tests/test_testing.py
+++ b/tests/test_testing.py
@@ -411,3 +411,18 @@ def test_cli_custom_obj(app):
     runner = app.test_cli_runner()
     runner.invoke(hello_command, obj=script_info)
     assert NS.called
+
+
+def test_client_pop_all_preserved(app, req_ctx, client):
+    @app.route("/")
+    def index():
+        # stream_with_context pushes a third context, preserved by client
+        return flask.Response(flask.stream_with_context("hello"))
+
+    # req_ctx fixture pushed an initial context, not marked preserved
+    with client:
+        # request pushes a second request context, preserved by client
+        client.get("/")
+
+    # only req_ctx fixture should still be pushed
+    assert flask._request_ctx_stack.top is req_ctx