diff --git a/app/mailers/conversation_reply_mailer.rb b/app/mailers/conversation_reply_mailer.rb
index f9572ba374e41..127231b9ab4d4 100644
--- a/app/mailers/conversation_reply_mailer.rb
+++ b/app/mailers/conversation_reply_mailer.rb
@@ -67,6 +67,10 @@ def should_use_conversation_email_address?
     @inbox.inbox_type == 'Email' || inbound_email_enabled?
   end
 
+  def should_use_inbox_from?
+    ENV['MAILER_SENDER_INBOX_PREFERENCE'] == 'true'
+  end
+
   def conversation_already_viewed?
     # whether contact already saw the message on widget
     return unless @conversation.contact_last_seen_at
@@ -101,8 +105,7 @@ def business_name
   end
 
   def from_email
-    sender_inbox_preference = ENV.fetch('MAILER_SENDER_INBOX_PREFERENCE', 'false') == 'true'
-    return parse_email(@account.support_email) if should_use_conversation_email_address? && !sender_inbox_preference
+    return parse_email(@account.support_email) if should_use_conversation_email_address? && !should_use_inbox_from?
 
     parse_email(inbox_from_email_address)
   end
diff --git a/app/mailers/conversation_reply_mailer_helper.rb b/app/mailers/conversation_reply_mailer_helper.rb
index 0499fb75dce6c..3a41e99df5778 100644
--- a/app/mailers/conversation_reply_mailer_helper.rb
+++ b/app/mailers/conversation_reply_mailer_helper.rb
@@ -81,12 +81,15 @@ def email_reply_to
 
   # Use channel email domain or account email domain depending on preference configuration for custom message_id and in_reply_to
   def channel_email_domain
-    use_inbox_email = ENV['MAILER_INBOUND_INBOX_PREFERENCE'] == 'true'
     inbox_email_domain = @inbox.channel.try(:email)&.split('@')&.last
-    return inbox_email_domain if inbox_email_domain.present? && use_inbox_email
+    return inbox_email_domain if inbox_email_domain.present? && should_use_channel_domain?
     return @account.inbound_email_domain if @account.inbound_email_domain.present?
     return inbox_email_domain if inbox_email_domain.present?
 
     raise(StandardError, 'Account inbound email domain and channel email domain not present.')
   end
+
+  def should_use_channel_domain?
+    ENV['MAILER_INBOUND_INBOX_PREFERENCE'] == 'true'
+  end
 end
diff --git a/spec/mailers/conversation_reply_mailer_spec.rb b/spec/mailers/conversation_reply_mailer_spec.rb
index e4bfac4139782..21eb32c5ccfa7 100644
--- a/spec/mailers/conversation_reply_mailer_spec.rb
+++ b/spec/mailers/conversation_reply_mailer_spec.rb
@@ -383,5 +383,37 @@
         expect(mail.in_reply_to).to eq("account/#{conversation.account.id}/conversation/#{conversation.uuid}@#{domain}")
       end
     end
+
+    context 'when prefer inbox emails configured' do
+      let(:new_account) { create(:account, domain: 'example.com') }
+      let!(:email_channel) { create(:channel_email, account: new_account, email: 'testing@channel.com') }
+      let!(:inbox) { create(:inbox, channel: email_channel, account: new_account, email_address: 'testing@inbox.com') }
+      let(:inbox_member) { create(:inbox_member, user: agent, inbox: inbox) }
+      let(:conversation) { create(:conversation, assignee: agent, inbox: inbox_member.inbox, account: new_account) }
+      let!(:message) { create(:message, conversation: conversation, account: new_account) }
+      let(:mail) { described_class.reply_with_summary(message.conversation, message.id).deliver_now }
+      let(:domain) { inbox.channel.email.split('@').last }
+
+      before do
+        allow(class_instance).to receive(:should_use_channel_domain?).and_return(true)
+        allow(class_instance).to receive(:should_use_inbox_from?).and_return(true)
+      end
+
+      it 'sets the correct custom message id' do
+        expect(mail.message_id).to eq("conversation/#{conversation.uuid}/messages/#{message.id}@#{domain}")
+      end
+
+      it 'sets the correct in reply to id' do
+        expect(mail.in_reply_to).to eq("account/#{conversation.account.id}/conversation/#{conversation.uuid}@#{domain}")
+      end
+
+      it 'sets reply to email to be based on the inbox domain' do
+        expect(mail.reply_to).to eq(["reply+#{message.conversation.uuid}@#{domain}"])
+      end
+
+      it 'sets from email to the inbox email address' do
+        expect(mail.from).to eq([inbox.email_address])
+      end
+    end
   end
 end