diff --git a/flask/app.py b/flask/app.py
index 91139773..f75dd818 100644
--- a/flask/app.py
+++ b/flask/app.py
@@ -833,6 +833,7 @@ class Flask(_PackageBoundObject):
             self.debug = bool(debug)
         options.setdefault('use_reloader', self.debug)
         options.setdefault('use_debugger', self.debug)
+        options.setdefault('passthrough_errors', True)
         try:
             run_simple(host, port, self, **options)
         finally:
diff --git a/flask/cli.py b/flask/cli.py
index 360ce12e..141c9eea 100644
--- a/flask/cli.py
+++ b/flask/cli.py
@@ -422,7 +422,8 @@ def run_command(info, host, port, reload, debugger, eager_loading,
             print(' * Forcing debug %s' % (info.debug and 'on' or 'off'))
 
     run_simple(host, port, app, use_reloader=reload,
-               use_debugger=debugger, threaded=with_threads)
+               use_debugger=debugger, threaded=with_threads,
+               passthrough_errors=True)
 
 
 @click.command('shell', short_help='Runs a shell in the app context.')
diff --git a/tests/test_basic.py b/tests/test_basic.py
index d22e9e5b..d7cc7a3f 100644
--- a/tests/test_basic.py
+++ b/tests/test_basic.py
@@ -1222,6 +1222,26 @@ def test_exception_propagation():
         t.join()
 
 
+@pytest.mark.parametrize('debug', [True, False])
+@pytest.mark.parametrize('use_debugger', [True, False])
+@pytest.mark.parametrize('use_reloader', [True, False])
+@pytest.mark.parametrize('propagate_exceptions', [None, True, False])
+def test_werkzeug_passthrough_errors(monkeypatch, debug, use_debugger,
+                                     use_reloader, propagate_exceptions):
+    rv = {}
+
+    # Mocks werkzeug.serving.run_simple method
+    def run_simple_mock(*args, **kwargs):
+        rv['passthrough_errors'] = kwargs.get('passthrough_errors')
+
+    app = flask.Flask(__name__)
+    monkeypatch.setattr(werkzeug.serving, 'run_simple', run_simple_mock)
+    app.config['PROPAGATE_EXCEPTIONS'] = propagate_exceptions
+    app.run(debug=debug, use_debugger=use_debugger, use_reloader=use_reloader)
+    # make sure werkzeug always passes errors through
+    assert rv['passthrough_errors']
+
+
 def test_max_content_length():
     app = flask.Flask(__name__)
     app.config['MAX_CONTENT_LENGTH'] = 64