diff --git a/ckan/config/middleware.py b/ckan/config/middleware.py
index a21d75f5dba..754457c31a6 100644
--- a/ckan/config/middleware.py
+++ b/ckan/config/middleware.py
@@ -245,11 +245,16 @@ def __getattr__(self, name):
 
 
 def make_flask_stack(conf, **app_conf):
-    """ This has to pass the flask app through all the same middleware that
-    Pylons used """
+    """
+    This passes the flask app through most of the same middleware that Pylons
+    uses.
+    """
+
+    debug = app_conf.get('debug', True)
 
     root = os.path.dirname(os.path.dirname(os.path.abspath(__file__)))
     app = CKANFlask(__name__)
+    app.debug = debug
     app.template_folder = os.path.join(root, 'templates')
     app.app_ctx_globals_class = CKAN_AppCtxGlobals
 
@@ -257,7 +262,6 @@ def make_flask_stack(conf, **app_conf):
 
     # secret key needed for flask-debug-toolbar
     app.config['SECRET_KEY'] = '<replace with a secret key>'
-    app.debug = True
     app.config['DEBUG_TB_INTERCEPT_REDIRECTS'] = False
     DebugToolbarExtension(app)
 
diff --git a/ckanext/example_flask_iroutes/tests/test_routes.py b/ckanext/example_flask_iroutes/tests/test_routes.py
index fa8110c76c8..e1feab9742f 100644
--- a/ckanext/example_flask_iroutes/tests/test_routes.py
+++ b/ckanext/example_flask_iroutes/tests/test_routes.py
@@ -37,11 +37,6 @@ def setup(self):
         self.app = helpers._get_test_app()
         flask_app = self._find_flask_app(self.app)
 
-        # Blueprints can't be registered after the app has been setup. For
-        # some reason, if debug is True, the app will have exited its initial
-        # state, and can't have new registrations. Set debug=False to ensure
-        # we can continue to register blueprints.
-        flask_app.debug = False
         # Install plugin and register its blueprint
         if not plugins.plugin_loaded('example_flask_iroutes'):
             plugins.load('example_flask_iroutes')