diff --git a/lib/galaxy/config/__init__.py b/lib/galaxy/config/__init__.py
index 5cae18bf10bd..deb877fafb43 100644
--- a/lib/galaxy/config/__init__.py
+++ b/lib/galaxy/config/__init__.py
@@ -511,10 +511,10 @@ def resolve(key):
             if not parent:  # base case: nothing else needs resolving
                 return path
             parent_path = resolve(parent)  # recursively resolve parent path
-            if path is not None:
+            if path:
                 path = os.path.join(parent_path, path)  # resolve path
             else:
-                path = parent_path  # or use parent path
+                log.warning("Trying to resolve path for the '%s' option but it's empty/None", key)
 
             setattr(self, key, path)  # update property
             _cache[key] = path  # cache it!
@@ -557,6 +557,8 @@ def get_path(current_path, initial_path):
             return current_path
 
         current_value = getattr(self, key)  # resolved path or list of resolved paths
+        if not current_value:
+            return
         if isinstance(current_value, list):
             initial_paths = listify(self._raw_config[key], do_strip=True)  # initial unresolved paths
             updated_paths = []
diff --git a/lib/galaxy/jobs/__init__.py b/lib/galaxy/jobs/__init__.py
index 3e9a306e4116..f55562de63b0 100644
--- a/lib/galaxy/jobs/__init__.py
+++ b/lib/galaxy/jobs/__init__.py
@@ -384,6 +384,8 @@ def __init__(self, app: MinimalManagerApp):
                             f" release of Galaxy. Please convert to YAML at {self.app.config.job_config_file} or"
                             f" explicitly set `job_config_file` to {job_config_file} to remove this message"
                         )
+                if not job_config_file:
+                    raise OSError()
                 if ".xml" in job_config_file:
                     tree = load(job_config_file)
                     job_config_dict = self.__parse_job_conf_xml(tree)
diff --git a/test/unit/config/test_path_graph.py b/test/unit/config/test_path_graph.py
index 02f33787081f..77afe7333c55 100644
--- a/test/unit/config/test_path_graph.py
+++ b/test/unit/config/test_path_graph.py
@@ -142,7 +142,7 @@ def test_resolves_to_invalid_type(monkeypatch):
 
 
 def test_resolves_with_empty_component(monkeypatch):
-    # A path can be None (root path is never None; may be asigned elsewhere)
+    # A path can be None (root path is never None; may be assigned elsewhere)
     mock_schema = {
         "path0": {
             "type": "str",
@@ -155,7 +155,7 @@ def test_resolves_with_empty_component(monkeypatch):
         "path2": {
             "type": "str",
             "default": "value2",
-            "path_resolves_to": "path1",
+            "path_resolves_to": "path0",
         },
     }
     monkeypatch.setattr(AppSchema, "_read_schema", lambda a, b: get_schema(mock_schema))
@@ -163,5 +163,5 @@ def test_resolves_with_empty_component(monkeypatch):
 
     config = BaseAppConfiguration()
     assert config.path0 == "value0"
-    assert config.path1 == "value0"
+    assert config.path1 is None
     assert config.path2 == "value0/value2"
diff --git a/test/unit/config/test_path_resolves_to.py b/test/unit/config/test_path_resolves_to.py
index 97953b3d0787..d7e7dd0918d6 100644
--- a/test/unit/config/test_path_resolves_to.py
+++ b/test/unit/config/test_path_resolves_to.py
@@ -132,21 +132,21 @@ def test_kwargs_relative_path_old_prefix_for_other_option(mock_init):
 
 def test_kwargs_relative_path_old_prefix_empty_after_strip(mock_init):
     # Expect: use value from kwargs, strip old prefix, then resolve
-    new_path1 = "old-config"
+    new_path1 = "old-config/foo"
     config = BaseAppConfiguration(path1=new_path1)
 
-    assert config.path1 == "my-config/"  # stripped of old prefix, then resolved
+    assert config.path1 == "my-config/foo"  # stripped of old prefix, then resolved
     assert config.path2 == "my-data/my-data-files"  # stripped of old prefix, then resolved
     assert config.path3 == "my-other-files"  # no change
 
 
 def test_kwargs_set_to_null(mock_init):
-    # Expected: allow overriding with null, then resolve
+    # Expected: allow overriding with null
     # This is not a common scenario, but it does happen: one example is
     # `job_config` set to `None` when testing
     config = BaseAppConfiguration(path1=None)
 
-    assert config.path1 == "my-config"  # resolved
+    assert config.path1 is None
     assert config.path2 == "my-data/my-data-files"  # resolved
     assert config.path3 == "my-other-files"  # no change