diff --git a/enterprise/app/jobs/captain/conversation/response_builder_job.rb b/enterprise/app/jobs/captain/conversation/response_builder_job.rb
index 9f8acc474..2967a8ce0 100644
--- a/enterprise/app/jobs/captain/conversation/response_builder_job.rb
+++ b/enterprise/app/jobs/captain/conversation/response_builder_job.rb
@@ -78,7 +78,7 @@ class Captain::Conversation::ResponseBuilderJob < ApplicationJob
   end
 
   def handoff_requested?
-    @response['response'] == 'conversation_handoff'
+    @response['action'] == 'handoff'
   end
 
   def process_action(action)
@@ -97,9 +97,10 @@ class Captain::Conversation::ResponseBuilderJob < ApplicationJob
   end
 
   def create_handoff_message
-    create_outgoing_message(
-      @assistant.config['handoff_message'].presence || I18n.t('conversations.captain.handoff')
-    )
+    handoff_message = @response['response'].presence ||
+                      @assistant.config['handoff_message'].presence ||
+                      I18n.t('conversations.captain.handoff')
+    create_outgoing_message(handoff_message)
   end
 
   def create_messages
diff --git a/enterprise/app/services/captain/assistant/agent_runner_service.rb b/enterprise/app/services/captain/assistant/agent_runner_service.rb
index 9c4e56841..b7eea59c7 100644
--- a/enterprise/app/services/captain/assistant/agent_runner_service.rb
+++ b/enterprise/app/services/captain/assistant/agent_runner_service.rb
@@ -95,7 +95,8 @@ class Captain::Assistant::AgentRunnerService
   def error_response(error_message)
     {
       'response' => 'conversation_handoff',
-      'reasoning' => "Error occurred: #{error_message}"
+      'reasoning' => "Error occurred: #{error_message}",
+      'action' => 'handoff'
     }
   end
 
diff --git a/enterprise/app/services/enterprise/message_templates/hook_execution_service.rb b/enterprise/app/services/enterprise/message_templates/hook_execution_service.rb
index 5c9a8a184..1560ce5ed 100644
--- a/enterprise/app/services/enterprise/message_templates/hook_execution_service.rb
+++ b/enterprise/app/services/enterprise/message_templates/hook_execution_service.rb
@@ -57,11 +57,13 @@ module Enterprise::MessageTemplates::HookExecutionService
     return unless conversation.pending?
 
     Rails.logger.info("Captain limit exceeded, performing handoff mid-conversation for conversation: #{conversation.id}")
+    handoff_message = inbox.captain_assistant&.config&.dig('handoff_message').presence ||
+                      'Transferring to another agent for further assistance.'
     conversation.messages.create!(
       message_type: :outgoing,
       account_id: conversation.account.id,
       inbox_id: conversation.inbox.id,
-      content: 'Transferring to another agent for further assistance.'
+      content: handoff_message
     )
     conversation.bot_handoff!
     send_out_of_office_message_after_handoff