diff --git a/app/controllers/profiles_controller.rb b/app/controllers/profiles_controller.rb
index f71e0a1302b..e4865642cd3 100644
--- a/app/controllers/profiles_controller.rb
+++ b/app/controllers/profiles_controller.rb
@@ -26,7 +26,15 @@ class ProfilesController < Profiles::ApplicationController
 
   def reset_private_token
     if current_user.reset_authentication_token!
-      flash[:notice] = "Token was successfully updated"
+      flash[:notice] = "Private token was successfully updated"
+    end
+
+    redirect_to profile_account_path
+  end
+
+  def reset_incoming_email_token
+    if current_user.reset_incoming_email_token!
+      flash[:notice] = "Incoming email token was successfully updated"
     end
 
     redirect_to profile_account_path
diff --git a/app/models/concerns/token_authenticatable.rb b/app/models/concerns/token_authenticatable.rb
index 24c7b26d223..04d30f46210 100644
--- a/app/models/concerns/token_authenticatable.rb
+++ b/app/models/concerns/token_authenticatable.rb
@@ -4,17 +4,21 @@ module TokenAuthenticatable
   private
 
   def write_new_token(token_field)
-    new_token = generate_token(token_field)
+    new_token = generate_available_token(token_field)
     write_attribute(token_field, new_token)
   end
 
-  def generate_token(token_field)
+  def generate_available_token(token_field)
     loop do
-      token = Devise.friendly_token
+      token = generate_token(token_field)
       break token unless self.class.unscoped.find_by(token_field => token)
     end
   end
 
+  def generate_token(token_field)
+    Devise.friendly_token
+  end
+
   class_methods do
     def authentication_token_fields
       @token_fields || []
diff --git a/app/models/project.rb b/app/models/project.rb
index 686d285410b..56b84b0aebb 100644
--- a/app/models/project.rb
+++ b/app/models/project.rb
@@ -624,13 +624,12 @@ class Project < ActiveRecord::Base
   end
 
   def new_issue_address(author)
-    # This feature is disabled for the time being.
-    return nil
+    return unless Gitlab::IncomingEmail.enabled? && author
 
-    if Gitlab::IncomingEmail.enabled? && author # rubocop:disable Lint/UnreachableCode
-      Gitlab::IncomingEmail.reply_address(
-        "#{path_with_namespace}+#{author.authentication_token}")
-    end
+    author.ensure_incoming_email_token!
+
+    Gitlab::IncomingEmail.reply_address(
+      "#{path_with_namespace}+#{author.incoming_email_token}")
   end
 
   def build_commit_note(commit)
diff --git a/app/models/user.rb b/app/models/user.rb
index 65e96ee6b2e..9a3619b0bc3 100644
--- a/app/models/user.rb
+++ b/app/models/user.rb
@@ -13,6 +13,7 @@ class User < ActiveRecord::Base
   DEFAULT_NOTIFICATION_LEVEL = :participating
 
   add_authentication_token_field :authentication_token
+  add_authentication_token_field :incoming_email_token
 
   default_value_for :admin, false
   default_value_for(:external) { current_application_settings.user_default_external }
@@ -119,7 +120,7 @@ class User < ActiveRecord::Base
   before_validation :set_public_email, if: ->(user) { user.public_email_changed? }
 
   after_update :update_emails_with_primary_email, if: ->(user) { user.email_changed? }
-  before_save :ensure_authentication_token
+  before_save :ensure_authentication_token, :ensure_incoming_email_token
   before_save :ensure_external_user_rights
   after_save :ensure_namespace_correct
   after_initialize :set_projects_limit
@@ -946,4 +947,13 @@ class User < ActiveRecord::Base
       signup_domain =~ regexp
     end
   end
+
+  def generate_token(token_field)
+    if token_field == :incoming_email_token
+      # Needs to be all lowercase and alphanumeric because it's gonna be used in an email address.
+      SecureRandom.hex
+    else
+      super
+    end
+  end
 end
diff --git a/app/views/profiles/accounts/show.html.haml b/app/views/profiles/accounts/show.html.haml
index e2e974ba072..2c256b1b233 100644
--- a/app/views/profiles/accounts/show.html.haml
+++ b/app/views/profiles/accounts/show.html.haml
@@ -8,24 +8,29 @@
 .row.prepend-top-default
   .col-lg-3.profile-settings-sidebar
     %h4.prepend-top-0
-      Private Token
+      Private Tokens
     %p
-      Your private token is used to access application resources without authentication.
+      Your private token is used to access the API and Atom feeds without
+      username/password authentication.
+    %p
+      Your incoming email token is used to create new issues by email, and is
+      included in your project-specific email addresses.
   .col-lg-9
-    = form_for @user, url: reset_private_token_profile_path, method: :put, html: { class: "private-token" } do |f|
-      %p.cgray
-        - if current_user.private_token
-          = label_tag "token", "Private token", class: "label-light"
-          = text_field_tag "token", current_user.private_token, class: "form-control"
-        - else
-          %span You don`t have one yet. Click generate to fix it.
+    %p.cgray
+      - if current_user.private_token
+        = label_tag "token", "Private token", class: "label-light"
+        = text_field_tag "token", current_user.private_token, class: "form-control"
+      - else
+        %span You don`t have one yet. Click generate to fix it.
       %p.help-block
-        It can be used for atom feeds or the API. Keep it secret!
-      .prepend-top-default
-        - if current_user.private_token
-          = f.submit 'Reset private token', data: { confirm: "Are you sure?" }, class: "btn btn-default"
-        - else
-          = f.submit 'Generate', class: "btn btn-default"
+        Keep this token secret, anyone with access to it can interact with the GitLab API as if they were you.
+    .prepend-top-default
+      - if current_user.private_token
+        = link_to 'Reset private token', reset_private_token_profile_path, method: :put, data: { confirm: "Are you sure?" }, class: "btn btn-default"
+      - else
+        = f.submit 'Generate', class: "btn btn-default"
+      = link_to 'Reset incoming email token', reset_incoming_email_token_profile_path, method: :put, data: { confirm: "Are you sure?" }, class: "btn btn-default"
+
 %hr
 .row.prepend-top-default
   .col-lg-3.profile-settings-sidebar
diff --git a/config/routes/profile.rb b/config/routes/profile.rb
index 4cb68c9b34a..52b9a565db8 100644
--- a/config/routes/profile.rb
+++ b/config/routes/profile.rb
@@ -4,6 +4,7 @@ resource :profile, only: [:show, :update] do
     get :applications, to: 'oauth/applications#index'
 
     put :reset_private_token
+    put :reset_incoming_email_token
     put :update_username
   end
 
diff --git a/db/migrate/20160819232256_add_incoming_email_token_to_users.rb b/db/migrate/20160819232256_add_incoming_email_token_to_users.rb
new file mode 100644
index 00000000000..f2cf956adc9
--- /dev/null
+++ b/db/migrate/20160819232256_add_incoming_email_token_to_users.rb
@@ -0,0 +1,16 @@
+# See http://doc.gitlab.com/ce/development/migration_style_guide.html
+# for more information on how to write migrations for GitLab.
+
+class AddIncomingEmailTokenToUsers < ActiveRecord::Migration
+  include Gitlab::Database::MigrationHelpers
+
+  # Set this constant to true if this migration requires downtime.
+  DOWNTIME = false
+
+  disable_ddl_transaction!
+
+  def change
+    add_column :users, :incoming_email_token, :string
+    add_concurrent_index :users, :incoming_email_token
+  end
+end
diff --git a/db/schema.rb b/db/schema.rb
index 5476b0c93e5..fd82fb326a6 100644
--- a/db/schema.rb
+++ b/db/schema.rb
@@ -11,7 +11,7 @@
 #
 # It's strongly recommended that you check this file into your version control system.
 
-ActiveRecord::Schema.define(version: 20161103171205) do
+ActiveRecord::Schema.define(version: 20160819232256) do
 
   # These are extensions that must be enabled in order to support this database
   enable_extension "plpgsql"
@@ -1176,6 +1176,7 @@ ActiveRecord::Schema.define(version: 20161103171205) do
     t.boolean "ldap_email", default: false, null: false
     t.boolean "external", default: false
     t.string "organization"
+    t.string   "incoming_email_token"
   end
 
   add_index "users", ["admin"], name: "index_users_on_admin", using: :btree
@@ -1185,6 +1186,7 @@ ActiveRecord::Schema.define(version: 20161103171205) do
   add_index "users", ["current_sign_in_at"], name: "index_users_on_current_sign_in_at", using: :btree
   add_index "users", ["email"], name: "index_users_on_email", unique: true, using: :btree
   add_index "users", ["email"], name: "index_users_on_email_trigram", using: :gin, opclasses: {"email"=>"gin_trgm_ops"}
+  add_index "users", ["incoming_email_token"], name: "index_users_on_incoming_email_token", using: :btree
   add_index "users", ["name"], name: "index_users_on_name", using: :btree
   add_index "users", ["name"], name: "index_users_on_name_trigram", using: :gin, opclasses: {"name"=>"gin_trgm_ops"}
   add_index "users", ["reset_password_token"], name: "index_users_on_reset_password_token", unique: true, using: :btree
diff --git a/lib/gitlab/email/handler/create_issue_handler.rb b/lib/gitlab/email/handler/create_issue_handler.rb
index 4e6566af8ab..9f90a3ec2b2 100644
--- a/lib/gitlab/email/handler/create_issue_handler.rb
+++ b/lib/gitlab/email/handler/create_issue_handler.rb
@@ -5,16 +5,16 @@ module Gitlab
   module Email
     module Handler
       class CreateIssueHandler < BaseHandler
-        attr_reader :project_path, :authentication_token
+        attr_reader :project_path, :incoming_email_token
 
         def initialize(mail, mail_key)
           super(mail, mail_key)
-          @project_path, @authentication_token =
+          @project_path, @incoming_email_token =
             mail_key && mail_key.split('+', 2)
         end
 
         def can_handle?
-          !authentication_token.nil?
+          !incoming_email_token.nil?
         end
 
         def execute
@@ -29,7 +29,7 @@ module Gitlab
         end
 
         def author
-          @author ||= User.find_by(authentication_token: authentication_token)
+          @author ||= User.find_by(incoming_email_token: incoming_email_token)
         end
 
         def project
diff --git a/spec/features/projects/issues/issues_spec.rb b/spec/features/projects/issues/issues_spec.rb
new file mode 100644
index 00000000000..e69de29bb2d
diff --git a/spec/fixtures/emails/wrong_authentication_token.eml b/spec/fixtures/emails/wrong_incoming_email_token.eml
similarity index 100%
rename from spec/fixtures/emails/wrong_authentication_token.eml
rename to spec/fixtures/emails/wrong_incoming_email_token.eml
diff --git a/spec/lib/gitlab/email/handler/create_issue_handler_spec.rb b/spec/lib/gitlab/email/handler/create_issue_handler_spec.rb
index a5cc7b02936..939189a3bc0 100644
--- a/spec/lib/gitlab/email/handler/create_issue_handler_spec.rb
+++ b/spec/lib/gitlab/email/handler/create_issue_handler_spec.rb
@@ -18,7 +18,7 @@ xdescribe Gitlab::Email::Handler::CreateIssueHandler, lib: true do
     create(
       :user,
       email: 'jake@adventuretime.ooo',
-      authentication_token: 'auth_token'
+      incoming_email_token: 'auth_token'
     )
   end
 
@@ -60,8 +60,8 @@ xdescribe Gitlab::Email::Handler::CreateIssueHandler, lib: true do
       end
     end
 
-    context "when we can't find the authentication_token" do
-      let(:email_raw) { fixture_file("emails/wrong_authentication_token.eml") }
+    context "when we can't find the incoming_email_token" do
+      let(:email_raw) { fixture_file("emails/wrong_incoming_email_token.eml") }
 
       it "raises an UserNotFoundError" do
         expect { receiver.execute }.to raise_error(Gitlab::Email::UserNotFoundError)