diff --git a/cypress/e2e/po/components/card.po.ts b/cypress/e2e/po/components/card.po.ts
index 050e545c9bb..c456dfd6c31 100644
--- a/cypress/e2e/po/components/card.po.ts
+++ b/cypress/e2e/po/components/card.po.ts
@@ -14,6 +14,10 @@ export default class CardPo extends ComponentPo {
     return this.self().get('[data-testid="card-body-slot"]');
   }
 
+  getError(): CypressChainable {
+    return this.self().get('[data-testid="card-body-slot"] > .text-error');
+  }
+
   getActionButton(): CypressChainable {
     return this.self().get('[data-testid="card-actions-slot"]');
   }
diff --git a/cypress/e2e/po/pages/global-settings/feature-flags.po.ts b/cypress/e2e/po/pages/global-settings/feature-flags.po.ts
index 9ba6893bddf..d04893e4755 100644
--- a/cypress/e2e/po/pages/global-settings/feature-flags.po.ts
+++ b/cypress/e2e/po/pages/global-settings/feature-flags.po.ts
@@ -54,6 +54,17 @@ export class FeatureFlagsPagePo extends RootClusterPage {
     return card.getBody().contains(label);
   }
 
+  /**
+   * Get card body error
+   * @param error
+   * @returns
+   */
+  cardActionError(error: string): CypressChainable {
+    const card = new CardPo();
+
+    return card.getError().contains(error);
+  }
+
   /**
    * Click action button
    * @param label Activate or Deactivate
diff --git a/cypress/e2e/tests/pages/global-settings/feature-flags.spec.ts b/cypress/e2e/tests/pages/global-settings/feature-flags.spec.ts
index 4e42709ddac..6ff0f77d3ad 100644
--- a/cypress/e2e/tests/pages/global-settings/feature-flags.spec.ts
+++ b/cypress/e2e/tests/pages/global-settings/feature-flags.spec.ts
@@ -191,6 +191,43 @@ describe('Feature Flags', { testIsolation: 'off' }, () => {
     sideNav.groups().contains('Legacy').should('not.exist');
   });
 
+  it('error when toggling a feature flag is handled correctly', { tags: ['@globalSettings', '@adminUser'] }, () => {
+    // Check Current State: should be disabled by default
+    FeatureFlagsPagePo.navTo();
+    featureFlagsPage.list().details('unsupported-storage-drivers', 0).should('include.text', 'Disabled');
+
+    // Intercept the request to change the feature flag and return an error - 403, permission denied
+    cy.intercept({
+      method:   'PUT',
+      pathname: '/v1/management.cattle.io.features/unsupported-storage-drivers',
+      times:    1,
+    }, {
+      statusCode: 403,
+      body:       {
+        type:    'error',
+        links:   {},
+        code:    'Forbidden',
+        message: 'User does not have permission'
+      }
+    }).as('updateFeatureFlag');
+
+    // Activate
+    featureFlagsPage.list().elementWithName('unsupported-storage-drivers').scrollIntoView().should('be.visible');
+    featureFlagsPage.list().clickRowActionMenuItem('unsupported-storage-drivers', 'Activate');
+    featureFlagsPage.cardActionButton('Activate').click();
+
+    cy.wait(`@updateFeatureFlag`).its('response.statusCode').should('eq', 403);
+
+    // Check Updated State: should be active
+    featureFlagsPage.list().details('unsupported-storage-drivers', 0).should('include.text', 'Disabled');
+
+    // Check error message is displayed
+    featureFlagsPage.cardActionError('User does not have permission');
+
+    // Press cancel
+    featureFlagsPage.cardActionButton('Cancel').click();
+  });
+
   it('standard user has only read access to Feature Flag page', { tags: ['@globalSettings', '@standardUser'] }, () => {
     // verify action menus are hidden for standard user
 
diff --git a/shell/list/management.cattle.io.feature.vue b/shell/list/management.cattle.io.feature.vue
index a49d1a87580..ab36928d781 100644
--- a/shell/list/management.cattle.io.feature.vue
+++ b/shell/list/management.cattle.io.feature.vue
@@ -95,6 +95,9 @@ export default {
   watch: {
     showPromptUpdate(show) {
       if (show) {
+        // Clear last error
+        this.error = null;
+
         this.showModal = true;
       } else {
         this.showModal = false;
@@ -140,7 +143,9 @@ export default {
         btnCB(true);
         this.close();
       } catch (err) {
-        this.error = err;
+        // An error occurred, so toggle back the value - the call failed, so the change was not made
+        this.update.spec.value = !this.update.enabled;
+        this.error = err.message || err;
         btnCB(false);
       }
     },