diff --git a/ui/app/abilities/job.js b/ui/app/abilities/job.js
index fbc8d982c6b3..892837658c72 100644
--- a/ui/app/abilities/job.js
+++ b/ui/app/abilities/job.js
@@ -1,5 +1,5 @@
 import AbstractAbility from './abstract';
-import { computed } from '@ember/object';
+import { computed, get } from '@ember/object';
 import { or } from '@ember/object/computed';
 
 export default class Job extends AbstractAbility {
@@ -9,7 +9,7 @@ export default class Job extends AbstractAbility {
   @or(
     'bypassAuthorization',
     'selfTokenIsManagement',
-    'policiesSupportRunning',
+    'specificNamespaceSupportsRunning',
     'policiesSupportScaling'
   )
   canScale;
@@ -27,8 +27,34 @@ export default class Job extends AbstractAbility {
   )
   canDispatch;
 
-  @computed('rulesForNamespace.@each.capabilities')
+  policyNamespacesIncludePermissions(policies = [], permissions = []) {
+    // For each policy record, extract all policies of all namespaces
+    const allNamespacePolicies = policies
+      .toArray()
+      .map((policy) => get(policy, 'rulesJSON.Namespaces'))
+      .flat()
+      .map((namespace = {}) => {
+        return namespace.Capabilities;
+      })
+      .flat()
+      .compact();
+
+    // Check for requested permissions
+    return allNamespacePolicies.some((policy) => {
+      return permissions.includes(policy);
+    });
+  }
+
+  @computed('token.selfTokenPolicies.[]')
   get policiesSupportRunning() {
+    return this.policyNamespacesIncludePermissions(
+      this.token.selfTokenPolicies,
+      ['submit-job']
+    );
+  }
+
+  @computed('rulesForNamespace.@each.capabilities')
+  get specificNamespaceSupportsRunning() {
     return this.namespaceIncludesCapability('submit-job');
   }
 
diff --git a/ui/app/adapters/job.js b/ui/app/adapters/job.js
index 8545b4aa39ec..08cc9b98e28c 100644
--- a/ui/app/adapters/job.js
+++ b/ui/app/adapters/job.js
@@ -30,7 +30,7 @@ export default class JobAdapter extends WatchableNamespaceIDs {
   }
 
   parse(spec) {
-    const url = addToPath(this.urlForFindAll('job'), '/parse');
+    const url = addToPath(this.urlForFindAll('job'), '/parse?namespace=*');
     return this.ajax(url, 'POST', {
       data: {
         JobHCL: spec,
diff --git a/ui/app/components/job-editor.js b/ui/app/components/job-editor.js
index 6b9d9da0d587..c2944e4a24f2 100644
--- a/ui/app/components/job-editor.js
+++ b/ui/app/components/job-editor.js
@@ -62,7 +62,8 @@ export default class JobEditor extends Component {
     try {
       yield this.job.parse();
     } catch (err) {
-      const error = messageFromAdapterError(err) || 'Could not parse input';
+      const error =
+        messageFromAdapterError(err, 'parse jobs') || 'Could not parse input';
       this.set('parseError', error);
       this.scrollToError();
       return;
@@ -72,7 +73,8 @@ export default class JobEditor extends Component {
       const plan = yield this.job.plan();
       this.set('planOutput', plan);
     } catch (err) {
-      const error = messageFromAdapterError(err) || 'Could not plan job';
+      const error =
+        messageFromAdapterError(err, 'plan jobs') || 'Could not plan job';
       this.set('planError', error);
       this.scrollToError();
     }
diff --git a/ui/tests/acceptance/jobs-list-test.js b/ui/tests/acceptance/jobs-list-test.js
index 59ea143a31bc..2a758f44a7b7 100644
--- a/ui/tests/acceptance/jobs-list-test.js
+++ b/ui/tests/acceptance/jobs-list-test.js
@@ -468,6 +468,37 @@ module('Acceptance | jobs list', function (hooks) {
     await JobsList.visit({ namespace: READ_AND_WRITE_NAMESPACE });
     assert.notOk(JobsList.runJobButton.isDisabled);
 
+    await JobsList.visit({ namespace: READ_ONLY_NAMESPACE });
+    assert.notOk(JobsList.runJobButton.isDisabled);
+  });
+
+  test('when the user has no client tokens that allow them to run a job', async function (assert) {
+    const READ_AND_WRITE_NAMESPACE = 'read-and-write-namespace';
+    const READ_ONLY_NAMESPACE = 'read-only-namespace';
+
+    server.create('namespace', { id: READ_ONLY_NAMESPACE });
+
+    const policy = server.create('policy', {
+      id: 'something',
+      name: 'something',
+      rulesJSON: {
+        Namespaces: [
+          {
+            Name: READ_ONLY_NAMESPACE,
+            Capabilities: ['list-job'],
+          },
+        ],
+      },
+    });
+
+    clientToken.policyIds = [policy.id];
+    clientToken.save();
+
+    window.localStorage.nomadTokenSecret = clientToken.secretId;
+
+    await JobsList.visit({ namespace: READ_AND_WRITE_NAMESPACE });
+    assert.ok(JobsList.runJobButton.isDisabled);
+
     await JobsList.visit({ namespace: READ_ONLY_NAMESPACE });
     assert.ok(JobsList.runJobButton.isDisabled);
   });
diff --git a/ui/tests/integration/components/job-editor-test.js b/ui/tests/integration/components/job-editor-test.js
index aab1e7973d63..05c121ff4d6a 100644
--- a/ui/tests/integration/components/job-editor-test.js
+++ b/ui/tests/integration/components/job-editor-test.js
@@ -177,7 +177,7 @@ module('Integration | Component | job-editor', function (hooks) {
     await planJob(spec);
     const requests = this.server.pretender.handledRequests.mapBy('url');
     assert.ok(
-      requests.includes('/v1/jobs/parse'),
+      requests.includes('/v1/jobs/parse?namespace=*'),
       'HCL job spec is parsed first'
     );
     assert.ok(
diff --git a/ui/tests/unit/abilities/job-test.js b/ui/tests/unit/abilities/job-test.js
index f1f89233bbf9..70e2c1eded45 100644
--- a/ui/tests/unit/abilities/job-test.js
+++ b/ui/tests/unit/abilities/job-test.js
@@ -251,19 +251,18 @@ module('Unit | Ability | job', function (hooks) {
     this.owner.register('service:token', mockToken);
 
     assert.ok(
-      this.can.cannot('run job', null, { namespace: 'production-web' })
+      this.can.can(
+        'run job',
+        null,
+        { namespace: 'production-web' },
+        'The existence of a single namespace where a job can be run means that can run is enabled'
+      )
     );
     assert.ok(this.can.can('run job', null, { namespace: 'production-api' }));
     assert.ok(this.can.can('run job', null, { namespace: 'production-other' }));
     assert.ok(
       this.can.can('run job', null, { namespace: 'something-suffixed' })
     );
-    assert.ok(
-      this.can.cannot('run job', null, {
-        namespace: 'something-more-suffixed',
-      }),
-      'expected the namespace with the greatest number of matched characters to be chosen'
-    );
     assert.ok(
       this.can.can('run job', null, { namespace: '000-abc-999' }),
       'expected to be able to match against more than one wildcard'
diff --git a/ui/tests/unit/adapters/job-test.js b/ui/tests/unit/adapters/job-test.js
index e34b3c8d79ab..534c22376d3a 100644
--- a/ui/tests/unit/adapters/job-test.js
+++ b/ui/tests/unit/adapters/job-test.js
@@ -522,7 +522,7 @@ module('Unit | Adapter | Job', function (hooks) {
     await this.subject().parse('job "name-goes-here" {');
 
     const request = this.server.pretender.handledRequests[0];
-    assert.equal(request.url, `/v1/jobs/parse?region=${region}`);
+    assert.equal(request.url, `/v1/jobs/parse?namespace=*&region=${region}`);
     assert.equal(request.method, 'POST');
     assert.deepEqual(JSON.parse(request.requestBody), {
       JobHCL: 'job "name-goes-here" {',