diff --git a/apps/meteor/app/integrations/server/methods/incoming/addIncomingIntegration.ts b/apps/meteor/app/integrations/server/methods/incoming/addIncomingIntegration.ts
index b755317c06945..869a2fc4c9121 100644
--- a/apps/meteor/app/integrations/server/methods/incoming/addIncomingIntegration.ts
+++ b/apps/meteor/app/integrations/server/methods/incoming/addIncomingIntegration.ts
@@ -84,12 +84,22 @@ export const addIncomingIntegration = async (userId: string, integration: INewIn
 
 	const user = await Users.findOneByUsername(integration.username, { projection: { _id: 1 } });
 
-	if (!user || !(await hasPermissionAsync(user._id, 'message-impersonate'))) {
+	if (!user) {
 		throw new Meteor.Error('error-invalid-user', 'Invalid user', {
 			method: 'addIncomingIntegration',
 		});
 	}
 
+	if (!(await hasPermissionAsync(user._id, 'message-impersonate'))) {
+		throw new Meteor.Error(
+			'error-user-lacks-message-impersonate-permission',
+			"User selected for the incoming integration lacks the 'message-impersonate' permission.",
+			{
+				method: 'addIncomingIntegration',
+			},
+		);
+	}
+
 	// Default to transpiling with Babel for backwards compatibility; integrations
 	// can opt-out per-record by setting `skipTranspile: true` (removed in 9.0.0).
 	const skipTranspile = integration.skipTranspile === true;
diff --git a/apps/meteor/app/integrations/server/methods/incoming/updateIncomingIntegration.ts b/apps/meteor/app/integrations/server/methods/incoming/updateIncomingIntegration.ts
index eabc9e56a8372..ba5155e64fc4c 100644
--- a/apps/meteor/app/integrations/server/methods/incoming/updateIncomingIntegration.ts
+++ b/apps/meteor/app/integrations/server/methods/incoming/updateIncomingIntegration.ts
@@ -145,12 +145,22 @@ export const updateIncomingIntegration = async (
 	const username = 'username' in integration ? integration.username : currentIntegration.username;
 	const user = await Users.findOneByUsername(username, { projection: { _id: 1, username: 1 } });
 
-	if (!user || !(await hasPermissionAsync(user._id, 'message-impersonate'))) {
+	if (!user) {
 		throw new Meteor.Error('error-invalid-post-as-user', 'Invalid Post As User', {
 			method: 'updateIncomingIntegration',
 		});
 	}
 
+	if (!(await hasPermissionAsync(user._id, 'message-impersonate'))) {
+		throw new Meteor.Error(
+			'error-user-lacks-message-impersonate-permission',
+			"User selected for the incoming integration lacks the 'message-impersonate' permission.",
+			{
+				method: 'updateIncomingIntegration',
+			},
+		);
+	}
+
 	const updatedIntegration = await Integrations.findOneAndUpdate(
 		{ _id: integrationId },
 		{
diff --git a/apps/meteor/tests/end-to-end/api/incoming-integrations.ts b/apps/meteor/tests/end-to-end/api/incoming-integrations.ts
index 151ffe79f6f35..faa157bfd041b 100644
--- a/apps/meteor/tests/end-to-end/api/incoming-integrations.ts
+++ b/apps/meteor/tests/end-to-end/api/incoming-integrations.ts
@@ -227,7 +227,10 @@ describe('[Incoming Integrations]', () => {
 					.expect(400)
 					.expect((res) => {
 						expect(res.body).to.have.property('success', false);
-						expect(res.body).to.have.property('error', 'Invalid user [error-invalid-user]');
+						expect(res.body).to.have.property(
+							'error',
+							"User selected for the incoming integration lacks the 'message-impersonate' permission. [error-user-lacks-message-impersonate-permission]",
+						);
 					});
 			});
 		});
@@ -965,7 +968,10 @@ describe('[Incoming Integrations]', () => {
 				})
 				.expect((res) => {
 					expect(res.body).to.have.property('success', false);
-					expect(res.body).to.have.property('error', 'Invalid Post As User [error-invalid-post-as-user]');
+					expect(res.body).to.have.property(
+						'error',
+						"User selected for the incoming integration lacks the 'message-impersonate' permission. [error-user-lacks-message-impersonate-permission]",
+					);
 				});
 		});
 
diff --git a/packages/i18n/src/locales/en.i18n.json b/packages/i18n/src/locales/en.i18n.json
index b29ec32dc1295..ebe586a20a676 100644
--- a/packages/i18n/src/locales/en.i18n.json
+++ b/packages/i18n/src/locales/en.i18n.json
@@ -6490,6 +6490,7 @@
   "error-user-is-not-activated": "User is not activated",
   "error-user-is-not-agent": "User is not an Omnichannel Agent",
   "error-user-is-offline": "User is offline",
+  "error-user-lacks-message-impersonate-permission": "User selected for the incoming integration lacks the 'message-impersonate' permission.",
   "error-user-limit-exceeded": "The number of users you are trying to invite to #channel_name exceeds the limit set by the administrator",
   "error-user-not-belong-to-department": "User does not belong to this department",
   "error-user-not-found": "User not found",