diff --git a/app/mailers/group_smtp_mailer.rb b/app/mailers/group_smtp_mailer.rb
index f8510deae34..44edec917c3 100644
--- a/app/mailers/group_smtp_mailer.rb
+++ b/app/mailers/group_smtp_mailer.rb
@@ -26,7 +26,7 @@ class GroupSmtpMailer < ActionMailer::Base
     delivery_options = {
       address: from_group.smtp_server,
       port: from_group.smtp_port,
-      domain: from_group.email_username.split('@').last,
+      domain: from_group.email_username_domain,
       user_name: from_group.email_username,
       password: from_group.email_password,
       authentication: GlobalSetting.smtp_authentication,
diff --git a/app/mailers/user_notifications.rb b/app/mailers/user_notifications.rb
index bfbce4e4aba..acd10a0451c 100644
--- a/app/mailers/user_notifications.rb
+++ b/app/mailers/user_notifications.rb
@@ -327,6 +327,7 @@ class UserNotifications < ActionMailer::Base
     opts[:show_category_in_subject] = false
     opts[:show_tags_in_subject] = false
     opts[:show_group_in_subject] = true if SiteSetting.group_in_subject
+    opts[:use_group_smtp_if_configured] = true
 
     # We use the 'user_posted' event when you are emailed a post in a PM.
     opts[:notification_type] = 'posted'
@@ -460,6 +461,7 @@ class UserNotifications < ActionMailer::Base
       notification_type: notification_type,
       use_invite_template: opts[:use_invite_template],
       use_topic_title_subject: use_topic_title_subject,
+      use_group_smtp_if_configured: opts[:use_group_smtp_if_configured],
       user: user
     }
 
@@ -485,6 +487,12 @@ class UserNotifications < ActionMailer::Base
     group_name = opts[:group_name]
     locale = user_locale(user)
 
+    # this gets set in MessageBuilder if it is nil here, we just want to be
+    # able to override it if the group has SMTP enabled
+    from_address = nil
+    delivery_method_options = nil
+    use_from_address_for_reply_to = false
+
     template = +"user_notifications.user_#{notification_type}"
     if post.topic.private_message?
       template << "_pm"
@@ -520,9 +528,48 @@ class UserNotifications < ActionMailer::Base
       show_tags_in_subject = tags.any? ? tags.join(" ") : nil
     end
 
+    group = post.topic.allowed_groups&.first
+
+    # If the group has IMAP enabled, then this will be handled by
+    # the Jobs::GroupSmtpEmail which is enqueued from the PostAlerter
+    #
+    # use_group_smtp_if_configured is used to ensure that no notifications
+    # expect for specific ones that we bless (such as user_private_message)
+    # accidentally get sent with the group SMTP settings.
+    if group.present? &&
+       group.smtp_enabled &&
+       !group.imap_enabled &&
+       SiteSetting.enable_smtp &&
+       opts[:use_group_smtp_if_configured]
+
+      port, enable_tls, enable_starttls_auto = EmailSettingsValidator.provider_specific_ssl_overrides(
+        group.smtp_server, group.smtp_port, group.smtp_ssl, group.smtp_ssl
+      )
+
+      # TODO (martin): Remove this once testing is over and this is more stable.
+      Rails.logger.warn("Using SMTP settings from group #{group.name} (#{group.id}) to send user notification for topic #{post.topic.id} and user #{user.id} (#{user.email})")
+
+      delivery_method_options = {
+        address: group.smtp_server,
+        port: port,
+        domain: group.email_username_domain,
+        user_name: group.email_username,
+        password: group.email_password,
+        authentication: GlobalSetting.smtp_authentication,
+        enable_starttls_auto: enable_starttls_auto
+      }
+
+      # We want from to be the same as the group's email_username, so if
+      # someone emails support@discourse.org they will get a reply from
+      # support@discourse.org and be able to email the SMTP email, which
+      # will forward the email back into Discourse and process/link it correctly.
+      use_from_address_for_reply_to = true
+      from_address = group.email_username
+    end
+
     if post.topic.private_message?
       subject_pm =
-        if opts[:show_group_in_subject] && group = post.topic.allowed_groups&.first
+        if opts[:show_group_in_subject] && group.present?
           if group.full_name
             "[#{group.full_name}] "
           else
@@ -664,7 +711,10 @@ class UserNotifications < ActionMailer::Base
       site_description: SiteSetting.site_description,
       site_title: SiteSetting.title,
       site_title_url_encoded: UrlHelper.encode_component(SiteSetting.title),
-      locale: locale
+      locale: locale,
+      delivery_method_options: delivery_method_options,
+      use_from_address_for_reply_to: use_from_address_for_reply_to,
+      from: from_address
     }
 
     unless translation_override_exists
diff --git a/app/models/group.rb b/app/models/group.rb
index c7313fa2c7d..4e95974feac 100644
--- a/app/models/group.rb
+++ b/app/models/group.rb
@@ -707,7 +707,10 @@ class Group < ActiveRecord::Base
   end
 
   def self.find_by_email(email)
-    self.where("string_to_array(incoming_email, '|') @> ARRAY[?]", Email.downcase(email)).first
+    self.where(
+      "email_username = :email OR string_to_array(incoming_email, '|') @> ARRAY[:email]",
+      email: Email.downcase(email)
+    ).first
   end
 
   def bulk_add(user_ids)
@@ -870,8 +873,17 @@ class Group < ActiveRecord::Base
     }
   end
 
+  def email_username_domain
+    email_username.split('@').last
+  end
+
+  def email_username_user
+    email_username.split('@').first
+  end
+
   def email_username_regex
-    user, domain = email_username.split('@')
+    user = email_username_user
+    domain = email_username_domain
     if user.present? && domain.present?
       /^#{Regexp.escape(user)}(\+[^@]*)?@#{Regexp.escape(domain)}$/i
     end
diff --git a/app/models/topic.rb b/app/models/topic.rb
index 5a07e58ea91..32c004ed0ad 100644
--- a/app/models/topic.rb
+++ b/app/models/topic.rb
@@ -1674,6 +1674,15 @@ class Topic < ActiveRecord::Base
       # group if the group is present. If combined addresses is empty we do
       # not need to do this check, and instead can proceed on to adding the
       # from address.
+      #
+      # Will not include test1@gmail.com if the only IncomingEmail
+      # is:
+      #
+      # from: test1@gmail.com
+      # to: test+support@discoursemail.com
+      #
+      # Because we don't care about the from addresses and also the to address
+      # is not the email_username, which will be something like test1@gmail.com.
       if group.present? && combined_addresses.any?
         next if combined_addresses.none? { |address| address =~ group.email_username_regex }
       end
diff --git a/app/services/post_alerter.rb b/app/services/post_alerter.rb
index 2958cea2986..86cf77f8291 100644
--- a/app/services/post_alerter.rb
+++ b/app/services/post_alerter.rb
@@ -588,13 +588,19 @@ class PostAlerter
     warn_if_not_sidekiq
 
     # Users who interacted with the post by _directly_ emailing the group
-    # via the group's email_username. This excludes people who replied via
-    # email to a user_private_message notification email. These people should
+    # via the group's email_username which is configured via SMTP/IMAP.
+    #
+    # This excludes people who replied via email to a user_private_message
+    # notification email which will have a PostReplyKey. These people should
     # not be emailed again by the user_private_message notifications below.
+    #
+    # This also excludes people who emailed the group by one of its incoming_email
+    # addresses, e.g. somegroup+support@discoursemail.com, which is part of the
+    # normal group email flow and has nothing to do with SMTP/IMAP.
     emails_to_skip_send = notify_group_direct_emailers(post)
 
     # Users that aren't part of any mentioned groups and who did not email
-    # the group directly.
+    # the group directly at the group's email_username.
     users = directly_targeted_users(post).reject { |u| notified.include?(u) }
     DiscourseEvent.trigger(:before_create_notifications_for_users, users, post)
     users.each do |user|
@@ -604,7 +610,7 @@ class PostAlerter
       end
     end
 
-    # Users that are part of all mentioned groups
+    # Users that are part of all mentioned groups.
     users = indirectly_targeted_users(post).reject { |u| notified.include?(u) }
     DiscourseEvent.trigger(:before_create_notifications_for_users, users, post)
     users.each do |user|
@@ -636,7 +642,7 @@ class PostAlerter
       end
     end
 
-    # Add the group's email into the array, because it is used for
+    # Add the group's email_username into the array, because it is used for
     # skip_send_email_to in the case of user private message notifications
     # (we do not want the group to be sent any emails from here because it
     # will make another email for IMAP to pick up in the group's mailbox)
diff --git a/lib/email/receiver.rb b/lib/email/receiver.rb
index b580e7ea408..5ec587ed377 100644
--- a/lib/email/receiver.rb
+++ b/lib/email/receiver.rb
@@ -952,7 +952,13 @@ module Email
     end
 
     def group_incoming_emails_regex
-      @group_incoming_emails_regex ||= Regexp.union Group.pluck(:incoming_email).select(&:present?).map { |e| e.split("|") }.flatten.uniq
+      @group_incoming_emails_regex = Regexp.union(
+        DB.query_single(<<~SQL).map { |e| e.split("|") }.flatten.compact_blank.uniq
+          SELECT CONCAT(incoming_email, '|', email_username)
+          FROM groups
+          WHERE incoming_email IS NOT NULL OR email_username IS NOT NULL
+        SQL
+      )
     end
 
     def category_email_in_regex
diff --git a/spec/components/email/receiver_spec.rb b/spec/components/email/receiver_spec.rb
index dec90fd99b8..636cc73cad5 100644
--- a/spec/components/email/receiver_spec.rb
+++ b/spec/components/email/receiver_spec.rb
@@ -968,6 +968,23 @@ describe Email::Receiver do
       include_examples "creates topic with forwarded message as quote", :group, "team@bar.com|meat@bar.com"
     end
 
+    context "when a reply is sent to a group's email_username" do
+      let!(:topic) do
+        group.update(email_username: "team@somesmtpaddress.com")
+        process(:email_reply_1)
+        Topic.last
+      end
+
+      it "does not invite the group email_username as a staged user" do
+        process(:email_reply_to_group_email_username)
+        expect(User.find_by_email("team@somesmtpaddress.com")).to eq(nil)
+      end
+
+      it "creates the reply when the sender and referenced messsage id are known" do
+        expect { process(:email_reply_to_group_email_username) }.to change { topic.posts.count }.by(1).and change { Topic.count }.by(0)
+      end
+    end
+
     context "when message sent to a group has no key and find_related_post_with_key is enabled" do
       let!(:topic) do
         process(:email_reply_1)
diff --git a/spec/components/imap/sync_spec.rb b/spec/components/imap/sync_spec.rb
index 7eac7ac6a33..04ee4eb3cde 100644
--- a/spec/components/imap/sync_spec.rb
+++ b/spec/components/imap/sync_spec.rb
@@ -20,8 +20,8 @@ describe Imap::Sync do
       :group,
       imap_server: 'imap.gmail.com',
       imap_port: 993,
-      email_username: 'discourse@example.com',
-      email_password: 'discourse@example.com',
+      email_username: 'groupemailusername@example.com',
+      email_password: 'password',
       imap_mailbox_name: '[Gmail]/All Mail'
     )
   end
diff --git a/spec/fixtures/emails/email_reply_to_group_email_username.eml b/spec/fixtures/emails/email_reply_to_group_email_username.eml
new file mode 100644
index 00000000000..f66aa37eea9
--- /dev/null
+++ b/spec/fixtures/emails/email_reply_to_group_email_username.eml
@@ -0,0 +1,12 @@
+Return-Path: <two@foo.com>
+From: Two <two@foo.com>
+To: team@somesmtpaddress.com
+Subject: RE: Testing email threading
+Date: Fri, 15 Jan 2016 00:12:43 +0100
+Message-ID: <44@foo.bar.mail>
+In-Reply-To: <34@foo.bar.mail>
+Mime-Version: 1.0
+Content-Type: text/plain
+Content-Transfer-Encoding: 7bit
+
+This is email reply **1**.
diff --git a/spec/mailers/user_notifications_spec.rb b/spec/mailers/user_notifications_spec.rb
index 3edb1f3b331..344cc55a8ff 100644
--- a/spec/mailers/user_notifications_spec.rb
+++ b/spec/mailers/user_notifications_spec.rb
@@ -611,6 +611,84 @@ describe UserNotifications do
       expect(mail.body).to include("[group1 (2)](http://test.localhost/groups/group1), [group2 (1)](http://test.localhost/groups/group2), [one](http://test.localhost/u/one), [two](http://test.localhost/u/two)")
     end
 
+    context "when group smtp is configured and SiteSetting.enable_smtp" do
+      let!(:group1) do
+        Fabricate(
+          :group,
+          name: "group1",
+          smtp_enabled: true,
+          smtp_port: 587,
+          smtp_ssl: true,
+          smtp_server: "smtp.test.com",
+          email_username: "user@test.com",
+          email_password: "password"
+        )
+      end
+
+      before do
+        SiteSetting.enable_smtp = true
+        topic.allowed_groups = [group1]
+      end
+
+      it "uses the from address, which is the group's email_username, for reply-to" do
+        mail = UserNotifications.user_private_message(
+          user,
+          post: response,
+          notification_type: notification.notification_type,
+          notification_data_hash: notification.data_hash
+        )
+
+        expect(mail.from).to eq([group1.email_username])
+        expect(mail.reply_to).to eq([group1.email_username])
+      end
+
+      it "uses the SMTP settings from the group for delivery" do
+        mail = UserNotifications.user_private_message(
+          user,
+          post: response,
+          notification_type: notification.notification_type,
+          notification_data_hash: notification.data_hash
+        )
+
+        delivery_method = mail.delivery_method.settings
+        expect(delivery_method[:port]).to eq(group1.smtp_port)
+        expect(delivery_method[:address]).to eq(group1.smtp_server)
+        expect(delivery_method[:domain]).to eq("test.com")
+        expect(delivery_method[:password]).to eq("password")
+        expect(delivery_method[:user_name]).to eq("user@test.com")
+      end
+
+      context "when imap is configured for the group" do
+        before do
+          group1.update(
+            imap_server: "imap.test.com",
+            imap_port: 993,
+            imap_ssl: true,
+            imap_enabled: true,
+            imap_mailbox_name: "All Mail"
+          )
+        end
+
+        it "does not use group SMTP settings for delivery, this is handled by Jobs::GroupSmtpEmail" do
+          mail = UserNotifications.user_private_message(
+            user,
+            post: response,
+            notification_type: notification.notification_type,
+            notification_data_hash: notification.data_hash
+          )
+
+          expect(mail.from).to eq([SiteSetting.notification_email])
+          expect(mail.reply_to).to eq([SiteSetting.notification_email])
+          delivery_method = mail.delivery_method.settings
+          expect(delivery_method[:port]).not_to eq(group1.smtp_port)
+          expect(delivery_method[:address]).not_to eq(group1.smtp_server)
+          expect(delivery_method[:domain]).not_to eq("test.com")
+          expect(delivery_method[:password]).not_to eq("password")
+          expect(delivery_method[:user_name]).not_to eq("user@test.com")
+        end
+      end
+    end
+
     context "when SiteSetting.group_name_in_subject is true" do
       before do
         SiteSetting.group_in_subject = true
diff --git a/spec/models/group_spec.rb b/spec/models/group_spec.rb
index 75630e524e3..a70bae19109 100644
--- a/spec/models/group_spec.rb
+++ b/spec/models/group_spec.rb
@@ -1291,4 +1291,20 @@ describe Group do
       expect(group.imap_updated_by).to eq(user)
     end
   end
+
+  describe "#find_by_email" do
+    it "finds the group by any of its incoming emails" do
+      group.update!(incoming_email: "abc@test.com|support@test.com")
+      expect(Group.find_by_email("abc@test.com")).to eq(group)
+      expect(Group.find_by_email("support@test.com")).to eq(group)
+      expect(Group.find_by_email("nope@test.com")).to eq(nil)
+    end
+
+    it "finds the group by its email_username" do
+      group.update!(email_username: "abc@test.com", incoming_email: "support@test.com")
+      expect(Group.find_by_email("abc@test.com")).to eq(group)
+      expect(Group.find_by_email("support@test.com")).to eq(group)
+      expect(Group.find_by_email("nope@test.com")).to eq(nil)
+    end
+  end
 end