diff --git a/lib/galaxy/jobs/runners/__init__.py b/lib/galaxy/jobs/runners/__init__.py
index dcd45eebb76b..dfc2f1aaa996 100644
--- a/lib/galaxy/jobs/runners/__init__.py
+++ b/lib/galaxy/jobs/runners/__init__.py
@@ -322,7 +322,7 @@ def _find_container(
         compute_job_directory=None
     ):
         if not compute_working_directory:
-            compute_working_directory = job_wrapper.working_directory
+            compute_working_directory = job_wrapper.tool_working_directory
 
         if not compute_tool_directory:
             compute_tool_directory = job_wrapper.tool.tool_dir
diff --git a/lib/galaxy/tools/deps/containers.py b/lib/galaxy/tools/deps/containers.py
index 35dfde5f38b2..12b2f3c879e6 100644
--- a/lib/galaxy/tools/deps/containers.py
+++ b/lib/galaxy/tools/deps/containers.py
@@ -298,7 +298,7 @@ def add_var(name, value):
             defaults = "$job_directory:ro,$tool_directory:ro,$job_directory/outputs:rw,$working_directory:rw"
         elif self.app_info.outputs_to_working_directory:
             # Should need default_file_path (which is a course estimate given
-            # object stores anyway.
+            # object stores anyway).
             defaults = "$galaxy_root:ro,$tool_directory:ro,$working_directory:rw,$default_file_path:ro"
         else:
             defaults = "$galaxy_root:ro,$tool_directory:ro,$working_directory:rw,$default_file_path:rw"
diff --git a/test/unit/jobs/test_runner_local.py b/test/unit/jobs/test_runner_local.py
index 53ee32b753c1..22012258951a 100644
--- a/test/unit/jobs/test_runner_local.py
+++ b/test/unit/jobs/test_runner_local.py
@@ -101,7 +101,8 @@ class MockJobWrapper( object ):
 
     def __init__( self, app, test_directory, tool ):
         working_directory = os.path.join( test_directory, "workdir" )
-        os.makedirs( working_directory )
+        tool_working_directory = os.path.join( working_directory, "working" )
+        os.makedirs( tool_working_directory )
         self.app = app
         self.tool = tool
         self.state = model.Job.states.QUEUED
@@ -112,6 +113,7 @@ def __init__( self, app, test_directory, tool ):
         self.write_version_cmd = None
         self.dependency_shell_commands = None
         self.working_directory = working_directory
+        self.tool_working_directory = tool_working_directory
         self.requires_setting_metadata = True
         self.job_destination = bunch.Bunch( id="default", params={} )
         self.galaxy_lib_dir = os.path.abspath( "lib" )