diff --git a/lib/galaxy/jobs/runners/__init__.py b/lib/galaxy/jobs/runners/__init__.py
index 095f6e3527b..de6aa6cb184 100644
--- a/lib/galaxy/jobs/runners/__init__.py
+++ b/lib/galaxy/jobs/runners/__init__.py
@@ -131,6 +131,11 @@ class BaseJobRunner(object):
                 method(arg)
             except Exception:
                 log.exception("(%s) Unhandled exception calling %s" % (job_id, name))
+                if not isinstance(arg, JobState):
+                    job_state = JobState(job_wrapper=arg, job_destination={})
+                else:
+                    job_state = arg
+                self.work_queue.put((self.fail_job, job_state))
 
     # Causes a runner's `queue_job` method to be called from a worker thread
     def put(self, job_wrapper):
diff --git a/test/integration/test_work_queue_put_failure.py b/test/integration/test_work_queue_put_failure.py
new file mode 100644
index 00000000000..b155d01abb3
--- /dev/null
+++ b/test/integration/test_work_queue_put_failure.py
@@ -0,0 +1,41 @@
+import tempfile
+
+from base import integration_util
+from base.populators import DatasetPopulator
+
+job_conf_yaml = """
+runners:
+  local:
+    load: galaxy.jobs.runners.pulsar:PulsarRESTJobRunner
+    workers: 1
+execution:
+  default: local
+  environments:
+    local:
+      runner: local
+"""
+
+
+class WorkQueuePutFailureTestCase(integration_util.IntegrationTestCase):
+
+    def setUp(self):
+        super(WorkQueuePutFailureTestCase, self).setUp()
+        self.dataset_populator = DatasetPopulator(self.galaxy_interactor)
+        self.history_id = self.dataset_populator.new_history()
+
+    @classmethod
+    def handle_galaxy_config_kwds(cls, config, ):
+        # config["jobs_directory"] = cls.jobs_directory
+        fd, path = tempfile.mkstemp(suffix='job_conf.yml')
+        with open(path, 'w') as job_conf:
+            job_conf.write(job_conf_yaml)
+        config["job_config_file"] = path
+        # Disable tool dependency resolution.
+        config["tool_dependency_dir"] = "none"
+
+    def test_job_fails(self):
+        self.dataset_populator.new_dataset(self.history_id, content="1 2 3")
+        self.dataset_populator.wait_for_history(self.history_id, assert_ok=False)
+        state_details = self.galaxy_interactor.get('histories/%s' % self.history_id).json()['state_details']
+        assert state_details['running'] == 0
+        assert state_details['error'] == 1