diff --git a/lib/galaxy/exceptions/__init__.py b/lib/galaxy/exceptions/__init__.py
index 8deab77bc17b..82f66efdbe7d 100644
--- a/lib/galaxy/exceptions/__init__.py
+++ b/lib/galaxy/exceptions/__init__.py
@@ -250,6 +250,11 @@ class InconsistentDatabase(MessageException):
     err_code = error_codes_by_name["INCONSISTENT_DATABASE"]
 
 
+class InconsistentApplicationState(MessageException):
+    status_code = 500
+    err_code = error_codes_by_name["INCONSISTENT_APPLICATION_STATE"]
+
+
 class InternalServerError(MessageException):
     status_code = 500
     err_code = error_codes_by_name["INTERNAL_SERVER_ERROR"]
diff --git a/lib/galaxy/exceptions/error_codes.json b/lib/galaxy/exceptions/error_codes.json
index 99464306acb6..e148b102b786 100644
--- a/lib/galaxy/exceptions/error_codes.json
+++ b/lib/galaxy/exceptions/error_codes.json
@@ -189,6 +189,11 @@
         "code": 500006,
         "message": "Reference data required for program execution failed to load."
     },
+    {
+        "name": "INCONSISTENT_APPLICATION_STATE",
+        "code": 500007,
+        "message": "Inconsistent application state (likely not dbms related) prevented fulfilling the request."
+    },
     {
         "name": "NOT_IMPLEMENTED",
         "code": 501001,
diff --git a/lib/tool_shed/managers/tools.py b/lib/tool_shed/managers/tools.py
index b9dc6209e1b3..0768758fc9bb 100644
--- a/lib/tool_shed/managers/tools.py
+++ b/lib/tool_shed/managers/tools.py
@@ -10,6 +10,7 @@
 
 from galaxy import exceptions
 from galaxy.exceptions import (
+    InconsistentApplicationState,
     InternalServerError,
     ObjectNotFound,
     RequestParameterInvalidException,
@@ -148,9 +149,17 @@ def _shed_tool_source_for(
         cloned_ok, error_message = clone_repository(repository_clone_url, work_dir, str(ctx.rev()))
         if error_message:
             raise InternalServerError("Failed to materialize target repository revision")
-        repo_files_dir = repository_metadata.repository.repo_path(trans.app)
+        repo_files_dir = repository_metadata.repository.hg_repository_path(trans.app.config.file_path)
+        if not repo_files_dir:
+            raise InconsistentApplicationState(
+                f"Failed to resolve repository path from hgweb_config_manager for [{trs_tool_id}], inconsistent repository state or application configuration"
+            )
         repo_rel_tool_path = relpath(tool_config, repo_files_dir)
         path_to_tool = os.path.join(work_dir, repo_rel_tool_path)
+        if not os.path.exists(path_to_tool):
+            raise InconsistentApplicationState(
+                f"Target tool expected at [{path_to_tool}] and not found, inconsistent repository state or application configuration"
+            )
         tool_source = get_tool_source(path_to_tool)
         return tool_source
     finally:
diff --git a/lib/tool_shed/util/repository_util.py b/lib/tool_shed/util/repository_util.py
index 9c9545c2e7f1..32829078f661 100644
--- a/lib/tool_shed/util/repository_util.py
+++ b/lib/tool_shed/util/repository_util.py
@@ -231,12 +231,7 @@ def create_repository(
     session = sa_session()
     with transaction(session):
         session.commit()
-    dir = os.path.join(app.config.file_path, *util.directory_hash_id(repository.id))
-    # Define repo name inside hashed directory.
-    final_repository_path = os.path.join(dir, "repo_%d" % repository.id)
-    # Create final repository directory.
-    if not os.path.exists(final_repository_path):
-        os.makedirs(final_repository_path)
+    final_repository_path = repository.ensure_hg_repository_path(app.config.file_path)
     os.rename(repository_path, final_repository_path)
     app.hgweb_config_manager.add_entry(lhs, final_repository_path)
     # Update the repository registry.
diff --git a/lib/tool_shed/webapp/model/__init__.py b/lib/tool_shed/webapp/model/__init__.py
index a31ab4861f4a..6edd97d4511a 100644
--- a/lib/tool_shed/webapp/model/__init__.py
+++ b/lib/tool_shed/webapp/model/__init__.py
@@ -524,6 +524,19 @@ def repo_path(self, app=None):
             os.path.join(hgweb_config_manager.hgweb_repo_prefix, self.user.username, self.name)
         )
 
+    def hg_repository_path(self, repositories_directory: str) -> str:
+        if self.id is None:
+            raise Exception("Attempting to call hg_repository_path before id has been set on repository object")
+        dir = os.path.join(repositories_directory, *util.directory_hash_id(self.id))
+        final_repository_path = os.path.join(dir, "repo_%d" % self.id)
+        return final_repository_path
+
+    def ensure_hg_repository_path(self, repositories_directory: str) -> str:
+        final_repository_path = self.hg_repository_path(repositories_directory)
+        if not os.path.exists(final_repository_path):
+            os.makedirs(final_repository_path)
+        return final_repository_path
+
     def revision(self):
         repo = self.hg_repo
         tip_ctx = repo[repo.changelog.tip()]