diff --git a/app/models/conversation.rb b/app/models/conversation.rb
index ca53238e8..6dd0e9df5 100644
--- a/app/models/conversation.rb
+++ b/app/models/conversation.rb
@@ -159,6 +159,7 @@ class Conversation < ApplicationRecord
   end
 
   def bot_handoff!
+    update(waiting_since: Time.current) if waiting_since.blank?
     open!
     dispatcher_dispatch(CONVERSATION_BOT_HANDOFF)
   end
diff --git a/enterprise/app/jobs/captain/conversation/response_builder_job.rb b/enterprise/app/jobs/captain/conversation/response_builder_job.rb
index 698ec56e7..c4723f6b9 100644
--- a/enterprise/app/jobs/captain/conversation/response_builder_job.rb
+++ b/enterprise/app/jobs/captain/conversation/response_builder_job.rb
@@ -42,10 +42,10 @@ class Captain::Conversation::ResponseBuilderJob < ApplicationJob
   end
 
   def process_response
-    ActiveRecord::Base.transaction do
-      if handoff_requested?
-        process_action('handoff')
-      else
+    if handoff_requested?
+      process_action('handoff')
+    else
+      ActiveRecord::Base.transaction do
         create_messages
         Rails.logger.info("[CAPTAIN][ResponseBuilderJob] Incrementing response usage for #{account.id}")
         account.increment_response_usage
diff --git a/spec/enterprise/jobs/captain/conversation/response_builder_job_spec.rb b/spec/enterprise/jobs/captain/conversation/response_builder_job_spec.rb
index 777086613..4e48eb355 100644
--- a/spec/enterprise/jobs/captain/conversation/response_builder_job_spec.rb
+++ b/spec/enterprise/jobs/captain/conversation/response_builder_job_spec.rb
@@ -92,6 +92,44 @@ RSpec.describe Captain::Conversation::ResponseBuilderJob, type: :job do
       end
     end
 
+    # Regression (PR #13417): wrapping create_handoff_message and bot_handoff! in the
+    # same transaction defers the message's after_create_commit until commit, at which
+    # point it clears waiting_since (bot_response). The handoff path must stay outside
+    # the transaction so the callback fires before bot_handoff! sets waiting_since.
+    context 'when handoff is requested' do
+      let(:conversation) { create(:conversation, inbox: inbox, account: account, status: :pending) }
+      let(:agent) { create(:user, account: account, role: :agent) }
+
+      before do
+        allow(account).to receive(:feature_enabled?).and_return(false)
+        allow(account).to receive(:feature_enabled?).with('captain_integration_v2').and_return(false)
+        allow(mock_llm_chat_service).to receive(:generate_response).and_return({ 'response' => 'conversation_handoff' })
+      end
+
+      it 'sets waiting_since to approximately the handoff time' do
+        freeze_time do
+          described_class.perform_now(conversation, assistant)
+
+          conversation.reload
+          expect(conversation.status).to eq('open')
+          expect(conversation.waiting_since).to be_within(1.second).of(Time.current)
+        end
+      end
+
+      it 'preserves waiting_since so a human reply consumes it for reply_time tracking' do
+        described_class.perform_now(conversation, assistant)
+
+        conversation.reload
+        expect(conversation.waiting_since).to be_present
+
+        # A human reply clears waiting_since (consumed by dispatch_create_events
+        # to emit FIRST_REPLY_CREATED or REPLY_CREATED for reply_time tracking).
+        create(:message, conversation: conversation, message_type: :outgoing,
+                         sender: agent, account: account, inbox: inbox)
+        expect(conversation.reload.waiting_since).to be_nil
+      end
+    end
+
     context 'when message contains an image' do
       let(:message_with_image) { create(:message, conversation: conversation, message_type: :incoming, content: 'Can you help with this error?') }
       let(:image_attachment) { message_with_image.attachments.create!(account: account, file_type: :image, external_url: 'https://example.com/error.jpg') }
diff --git a/spec/models/conversation_spec.rb b/spec/models/conversation_spec.rb
index e1883b54d..89c090207 100644
--- a/spec/models/conversation_spec.rb
+++ b/spec/models/conversation_spec.rb
@@ -313,6 +313,47 @@ RSpec.describe Conversation do
     end
   end
 
+  describe '#bot_handoff!' do
+    let(:conversation) { create(:conversation, status: :pending) }
+
+    before do
+      allow(Rails.configuration.dispatcher).to receive(:dispatch)
+    end
+
+    context 'when waiting_since is blank' do
+      before { conversation.update(waiting_since: nil) }
+
+      it 'sets waiting_since to current time' do
+        freeze_time do
+          conversation.bot_handoff!
+          expect(conversation.reload.waiting_since).to eq(Time.current)
+        end
+      end
+    end
+
+    context 'when waiting_since is already set' do
+      let(:original_time) { 1.hour.ago }
+
+      before { conversation.update(waiting_since: original_time) }
+
+      it 'preserves existing waiting_since' do
+        conversation.bot_handoff!
+        expect(conversation.reload.waiting_since).to be_within(1.second).of(original_time)
+      end
+    end
+
+    it 'changes status to open' do
+      conversation.bot_handoff!
+      expect(conversation.reload.status).to eq('open')
+    end
+
+    it 'dispatches CONVERSATION_BOT_HANDOFF event' do
+      expect(Rails.configuration.dispatcher).to receive(:dispatch)
+        .with(described_class::CONVERSATION_BOT_HANDOFF, anything, hash_including(conversation: conversation))
+      conversation.bot_handoff!
+    end
+  end
+
   describe '#toggle_priority' do
     it 'defaults priority to nil when created' do
       conversation = create(:conversation, status: 'open')