diff --git a/lib/galaxy/config.py b/lib/galaxy/config.py
index 8fac06f69cd..8a927244cdd 100644
--- a/lib/galaxy/config.py
+++ b/lib/galaxy/config.py
@@ -203,7 +203,7 @@ class Configuration(object):
             tempfile.tempdir = self.new_file_path
         self.shared_home_dir = kwargs.get("shared_home_dir", None)
         self.openid_consumer_cache_path = resolve_path(kwargs.get("openid_consumer_cache_path", "database/openid_consumer_cache"), self.root)
-        self.cookie_path = kwargs.get("cookie_path", "/")
+        self.cookie_path = kwargs.get("cookie_path", None)
         self.enable_quotas = string_as_bool(kwargs.get('enable_quotas', False))
         self.enable_unique_workflow_defaults = string_as_bool(kwargs.get('enable_unique_workflow_defaults', False))
         self.tool_path = resolve_path(kwargs.get("tool_path", "tools"), self.root)
diff --git a/lib/galaxy/visualization/plugins/interactive_environments.py b/lib/galaxy/visualization/plugins/interactive_environments.py
index d3131cba7ba..26571e31d6c 100644
--- a/lib/galaxy/visualization/plugins/interactive_environments.py
+++ b/lib/galaxy/visualization/plugins/interactive_environments.py
@@ -88,7 +88,7 @@ class InteractiveEnvironmentRequest(object):
             self.attr.proxy_prefix = '/'.join(
                 (
                     '',
-                    self.attr.galaxy_config.cookie_path.strip('/'),
+                    (self.attr.galaxy_config.cookie_path or '/').strip('/'),
                     self.attr.galaxy_config.dynamic_proxy_prefix.strip('/'),
                     self.attr.viz_id,
                 )
diff --git a/lib/galaxy/web/framework/webapp.py b/lib/galaxy/web/framework/webapp.py
index 95662602a6d..2ac12204139 100644
--- a/lib/galaxy/web/framework/webapp.py
+++ b/lib/galaxy/web/framework/webapp.py
@@ -625,7 +625,7 @@ class GalaxyWebTransaction(base.DefaultWebTransaction,
         Update the session cookie to match the current session.
         """
         self.set_cookie(self.security.encode_guid(self.galaxy_session.session_key),
-                        name=name, path=self.app.config.cookie_path)
+                        name=name, path=self.app.config.cookie_path or url_for('/'))
 
     def check_user_library_import_dir(self, user):
         if getattr(self.app.config, "user_library_import_dir_auto_creation", False):
diff --git a/lib/galaxy/web/proxy/__init__.py b/lib/galaxy/web/proxy/__init__.py
index 4702c5c277d..94c73335b2c 100644
--- a/lib/galaxy/web/proxy/__init__.py
+++ b/lib/galaxy/web/proxy/__init__.py
@@ -148,7 +148,7 @@ class GolangProxyLauncher(object):
                 config.dynamic_proxy_bind_port,
             ),
             "--listenPath", "/".join((
-                config.cookie_path,
+                (config.cookie_path or '/'),
                 config.dynamic_proxy_prefix
             )),
             "--cookieName", "galaxysession",
diff --git a/lib/galaxy/webapps/reports/config.py b/lib/galaxy/webapps/reports/config.py
index 89a9373476e..7f44096bb9a 100644
--- a/lib/galaxy/webapps/reports/config.py
+++ b/lib/galaxy/webapps/reports/config.py
@@ -48,7 +48,7 @@ class Configuration(object):
         self.blog_url = kwargs.get('blog_url', None)
         self.screencasts_url = kwargs.get('screencasts_url', None)
         self.log_events = False
-        self.cookie_path = kwargs.get("cookie_path", "/")
+        self.cookie_path = kwargs.get("cookie_path", None)
         # Error logging with sentry
         self.sentry_dsn = kwargs.get('sentry_dsn', None)
 
diff --git a/lib/galaxy/webapps/tool_shed/config.py b/lib/galaxy/webapps/tool_shed/config.py
index 8fef0ca1944..412ee196c49 100644
--- a/lib/galaxy/webapps/tool_shed/config.py
+++ b/lib/galaxy/webapps/tool_shed/config.py
@@ -66,7 +66,7 @@ class Configuration(object):
         # Where dataset files are stored
         self.file_path = resolve_path(kwargs.get("file_path", "database/community_files"), self.root)
         self.new_file_path = resolve_path(kwargs.get("new_file_path", "database/tmp"), self.root)
-        self.cookie_path = kwargs.get("cookie_path", "/")
+        self.cookie_path = kwargs.get("cookie_path", None)
         self.enable_quotas = string_as_bool(kwargs.get('enable_quotas', False))
         self.id_secret = kwargs.get("id_secret", "changethisinproductiontoo")
         # Tool stuff