diff --git a/ui/app/routes/jobs/job/definition.js b/ui/app/routes/jobs/job/definition.js
index f6294ebf5..4be568a11 100644
--- a/ui/app/routes/jobs/job/definition.js
+++ b/ui/app/routes/jobs/job/definition.js
@@ -1,8 +1,18 @@
 import Route from '@ember/routing/route';
+import EmberError from '@ember/error';
 
 export default Route.extend({
   model() {
     const job = this.modelFor('jobs.job');
+
+    // If there is no job, then there is no task group, so handle this as a 404
+    if (!job) {
+      const err = new EmberError(`Job for task group ${name} not found`);
+      err.code = '404';
+      this.controllerFor('application').set('error', err);
+      return;
+    }
+
     return job.fetchRawDefinition().then(definition => ({
       job,
       definition,
diff --git a/ui/tests/acceptance/job-definition-test.js b/ui/tests/acceptance/job-definition-test.js
index 78f65541b..18dbb3982 100644
--- a/ui/tests/acceptance/job-definition-test.js
+++ b/ui/tests/acceptance/job-definition-test.js
@@ -82,3 +82,18 @@ test('when changes are submitted, the site redirects to the job overview page',
     assert.equal(currentURL(), `/jobs/${job.id}`, 'Now on the job overview page');
   });
 });
+
+test('when the job for the definition is not found, an error message is shown, but the URL persists', function(assert) {
+  Definition.visit({ id: 'not-a-real-job' });
+
+  andThen(() => {
+    assert.equal(
+      server.pretender.handledRequests.findBy('status', 404).url,
+      '/v1/job/not-a-real-job',
+      'A request to the nonexistent job is made'
+    );
+    assert.equal(currentURL(), '/jobs/not-a-real-job/definition', 'The URL persists');
+    assert.ok(Definition.error.isPresent, 'Error message is shown');
+    assert.equal(Definition.error.title, 'Not Found', 'Error message is for 404');
+  });
+});
diff --git a/ui/tests/pages/jobs/job/definition.js b/ui/tests/pages/jobs/job/definition.js
index b015019b7..16272040b 100644
--- a/ui/tests/pages/jobs/job/definition.js
+++ b/ui/tests/pages/jobs/job/definition.js
@@ -1,4 +1,4 @@
-import { create, isPresent, visitable, clickable } from 'ember-cli-page-object';
+import { create, isPresent, visitable, clickable, text } from 'ember-cli-page-object';
 
 import jobEditor from 'nomad-ui/tests/pages/components/job-editor';
 
@@ -9,4 +9,11 @@ export default create({
   editor: jobEditor(),
 
   edit: clickable('[data-test-edit-job]'),
+
+  error: {
+    isPresent: isPresent('[data-test-error]'),
+    title: text('[data-test-error-title]'),
+    message: text('[data-test-error-message]'),
+    seekHelp: clickable('[data-test-error-message] a'),
+  },
 });