diff --git a/awx/ui/client/src/shared/form-generator.js b/awx/ui/client/src/shared/form-generator.js
index b18e9a5397..f9e1b9e426 100644
--- a/awx/ui/client/src/shared/form-generator.js
+++ b/awx/ui/client/src/shared/form-generator.js
@@ -1041,6 +1041,15 @@ angular.module('FormGenerator', [GeneratorHelpers.name, 'Utilities', listGenerat
                             };
                         }
 
+                        if (field.onError) {
+                            labelOptions.onError = {
+                                id: `${this.form.name}_${fld}_error_text`,
+                                ngShow: field.onError.ngShow,
+                                ngModel: field.onError.variable,
+                                text: field.onError.text
+                            };
+                        }
+
                         html += label(labelOptions);
 
                         html += "<div ";
@@ -1091,7 +1100,11 @@ angular.module('FormGenerator', [GeneratorHelpers.name, 'Utilities', listGenerat
                                 }
                                 html += "</div>\n";
                         }
+                        if (field.label === "Labels") {
+                            html += `<div class="error" id="${field.onError.id}" ng-show="${field.onError.ngShow}">${field.onError.text}</div>`;
+                        }
                         html += "<div class=\"error api-error\" id=\"" + this.form.name + "-" + fld + "-api-error\" ng-bind=\"" + fld + "_api_error\"></div>\n";
+                        
 
                         // Add help panel(s)
                         html += (field.helpCollapse) ? this.buildHelpCollapse(field.helpCollapse) : '';
@@ -2021,5 +2034,6 @@ angular.module('FormGenerator', [GeneratorHelpers.name, 'Utilities', listGenerat
                     ${options.text}
                 </label> `;
         }
+
     }
 ]);
diff --git a/awx/ui/client/src/templates/job_templates/add-job-template/job-template-add.controller.js b/awx/ui/client/src/templates/job_templates/add-job-template/job-template-add.controller.js
index d25d41e706..a51213251d 100644
--- a/awx/ui/client/src/templates/job_templates/add-job-template/job-template-add.controller.js
+++ b/awx/ui/client/src/templates/job_templates/add-job-template/job-template-add.controller.js
@@ -495,5 +495,51 @@
             $scope.formCancel = function () {
                 $state.transitionTo('templates');
             };
+
+            let handleLabelCount = () => {
+                /**
+                 * This block of code specifically handles the client-side validation of the `labels` field.
+                 * Due to it's detached nature in relation to the other job template fields, we must 
+                 * validate this field client-side in order to avoid the edge case where a user can make a 
+                 * successful POST to the `job_templates` endpoint but however encounter a 200 error from 
+                 * the `labels` endpoint due to a character limit.
+                 * 
+                 * We leverage two of select2's available events, `select` and `unselect`, to detect when the user
+                 * has either added or removed a label. From there, we set a flag and do simple string length
+                 * checks to make sure a label's chacacter count remains under 512. Otherwise, we disable the "Save" button
+                 * by invalidating the field and inform the user of the error.
+                */
+
+
+                $scope.job_template_labels_isValid = true;
+                const maxCount = 512;
+                const jt_label_id = 'job_template_labels';
+
+                // Detect when a new label is added
+                $(`#${jt_label_id}`).on('select2:select', (e) => {
+                    const { text } = e.params.data;
+
+                    // If the character count of an added label is greater than 512, we set `labels` field as invalid
+                    if (text.length > maxCount) {
+                        $scope.job_template_form.labels.$setValidity(`${jt_label_id}`, false);
+                        $scope.job_template_labels_isValid = false;
+                    }
+                });
+
+                // Detect when a label is removed
+                $(`#${jt_label_id}`).on('select2:unselect', (e) => {
+                    const maxCount = 512;
+                    const { text } = e.params.data;
+
+                    /* If the character count of a removed label is greater than 512 AND the field is currently marked
+                       as invalid, we set it back to valid */
+                    if (text.length > maxCount && $scope.job_template_form.labels.$error) {
+                        $scope.job_template_form.labels.$setValidity(`${jt_label_id}`, true);
+                        $scope.job_template_labels_isValid = true;
+                    }
+                });
+            };
+
+            handleLabelCount();
         }
     ];
diff --git a/awx/ui/client/src/templates/job_templates/edit-job-template/job-template-edit.controller.js b/awx/ui/client/src/templates/job_templates/edit-job-template/job-template-edit.controller.js
index 41528a57d8..cf5977baa3 100644
--- a/awx/ui/client/src/templates/job_templates/edit-job-template/job-template-edit.controller.js
+++ b/awx/ui/client/src/templates/job_templates/edit-job-template/job-template-edit.controller.js
@@ -704,5 +704,51 @@ export default
             $scope.formCancel = function () {
                 $state.go('templates');
             };
+
+            let handleLabelCount = () => {
+                /**
+                 * This block of code specifically handles the client-side validation of the `labels` field.
+                 * Due to it's detached nature in relation to the other job template fields, we must 
+                 * validate this field client-side in order to avoid the edge case where a user can make a 
+                 * successful POST to the `job_templates` endpoint but however encounter a 200 error from 
+                 * the `labels` endpoint due to a character limit.
+                 * 
+                 * We leverage two of select2's available events, `select` and `unselect`, to detect when the user
+                 * has either added or removed a label. From there, we set a flag and do simple string length
+                 * checks to make sure a label's chacacter count remains under 512. Otherwise, we disable the "Save" button
+                 * by invalidating the field and inform the user of the error.
+                */
+
+
+                $scope.job_template_labels_isValid = true;
+                const maxCount = 512;
+                const jt_label_id = 'job_template_labels';
+
+                // Detect when a new label is added
+                $(`#${jt_label_id}`).on('select2:select', (e) => {
+                    const { text } = e.params.data;
+
+                    // If the character count of an added label is greater than 512, we set `labels` field as invalid
+                    if (text.length > maxCount) {
+                        $scope.job_template_form.labels.$setValidity(`${jt_label_id}`, false);
+                        $scope.job_template_labels_isValid = false;
+                    }
+                });
+
+                // Detect when a label is removed
+                $(`#${jt_label_id}`).on('select2:unselect', (e) => {
+                    const maxCount = 512;
+                    const { text } = e.params.data;
+
+                    /* If the character count of a removed label is greater than 512 AND the field is currently marked
+                       as invalid, we set it back to valid */
+                    if (text.length > maxCount && $scope.job_template_form.labels.$error) {
+                        $scope.job_template_form.labels.$setValidity(`${jt_label_id}`, true);
+                        $scope.job_template_labels_isValid = true;
+                    }
+                });
+            };
+
+            handleLabelCount();
         }
     ];
diff --git a/awx/ui/client/src/templates/job_templates/job-template.form.js b/awx/ui/client/src/templates/job_templates/job-template.form.js
index d87d3c603e..7b75e16415 100644
--- a/awx/ui/client/src/templates/job_templates/job-template.form.js
+++ b/awx/ui/client/src/templates/job_templates/job-template.form.js
@@ -229,6 +229,10 @@ function(NotificationsList, i18n) {
                     dataPlacement: 'right',
                     awPopOver: "<p>" + i18n._("Optional labels that describe this job template, such as 'dev' or 'test'. Labels can be used to group and filter job templates and completed jobs.") + "</p>",
                     dataContainer: 'body',
+                    onError: {
+                        ngShow: 'job_template_labels_isValid !== true',
+                        text: i18n._('Max 512 characters per label.'),
+                    },
                     ngDisabled: '!(job_template_obj.summary_fields.user_capabilities.edit || canAddJobTemplate)'
                 },
                 custom_virtualenv: {