diff --git a/Gemfile b/Gemfile
index 46deda1f21..5164f4c908 100644
--- a/Gemfile
+++ b/Gemfile
@@ -3,7 +3,8 @@ source 'https://rubygems.org/'
 group :base do
   gem 'json', '= 2.5.1'
   gem 'mime-types', '1.25'
-  gem 'rack', '< 2.0'
+  gem 'rack', '>= 3'
+  gem 'rackup', '>= 2.1'
   gem 'rake', '< 13.0.0'
   gem 'rspec', '~> 3.0.0'
   gem 'rspec-collection_matchers'
diff --git a/Gemfile.lock b/Gemfile.lock
index fa637e6fc0..d37fd2ae33 100644
--- a/Gemfile.lock
+++ b/Gemfile.lock
@@ -4,7 +4,10 @@ GEM
     diff-lcs (1.5.0)
     json (2.5.1)
     mime-types (1.25)
-    rack (1.6.13)
+    rack (3.0.8)
+    rackup (2.1.0)
+      rack (>= 3)
+      webrick (~> 1.8)
     rake (12.3.3)
     rspec (3.0.0)
       rspec-core (~> 3.0.0)
@@ -28,9 +31,12 @@ PLATFORMS
 DEPENDENCIES
   json (= 2.5.1)
   mime-types (= 1.25)
-  rack (< 2.0)
+  rack (>= 3)
+  rackup (>= 2.1)
   rake (< 13.0.0)
   rspec (~> 3.0.0)
   rspec-collection_matchers
   webrick (~> 1.8.1)
 
+BUNDLED WITH
+   2.4.21
diff --git a/passenger.gemspec b/passenger.gemspec
index b13a3c8428..19900c6384 100644
--- a/passenger.gemspec
+++ b/passenger.gemspec
@@ -24,6 +24,7 @@ Gem::Specification.new do |s|
   }
   s.add_dependency 'rake', '>= 0.8.1'
   s.add_dependency 'rack'
+  s.add_dependency 'rackup'
   s.files = Dir[*PhusionPassenger::Packaging::GLOB] -
     Dir[*PhusionPassenger::Packaging::EXCLUDE_GLOB]
   s.executables = PhusionPassenger::Packaging::USER_EXECUTABLES +
diff --git a/src/ruby_supportlib/phusion_passenger/rack/handler.rb b/src/ruby_supportlib/phusion_passenger/rack/handler.rb
new file mode 100644
index 0000000000..d6f36559f7
--- /dev/null
+++ b/src/ruby_supportlib/phusion_passenger/rack/handler.rb
@@ -0,0 +1,71 @@
+# frozen_string_literal: true
+
+#  Phusion Passenger - https://www.phusionpassenger.com/
+#  Copyright (c) 2010-2017 Phusion Holding B.V.
+#
+#  "Passenger", "Phusion Passenger" and "Union Station" are registered
+#  trademarks of Phusion Holding B.V.
+#
+#  Permission is hereby granted, free of charge, to any person obtaining a copy
+#  of this software and associated documentation files (the "Software"), to deal
+#  in the Software without restriction, including without limitation the rights
+#  to use, copy, modify, merge, publish, distribute, sublicense, and/or sell
+#  copies of the Software, and to permit persons to whom the Software is
+#  furnished to do so, subject to the following conditions:
+#
+#  The above copyright notice and this permission notice shall be included in
+#  all copies or substantial portions of the Software.
+#
+#  THE SOFTWARE IS PROVIDED "AS IS", WITHOUT WARRANTY OF ANY KIND, EXPRESS OR
+#  IMPLIED, INCLUDING BUT NOT LIMITED TO THE WARRANTIES OF MERCHANTABILITY,
+#  FITNESS FOR A PARTICULAR PURPOSE AND NONINFRINGEMENT. IN NO EVENT SHALL THE
+#  AUTHORS OR COPYRIGHT HOLDERS BE LIABLE FOR ANY CLAIM, DAMAGES OR OTHER
+#  LIABILITY, WHETHER IN AN ACTION OF CONTRACT, TORT OR OTHERWISE, ARISING FROM,
+#  OUT OF OR IN CONNECTION WITH THE SOFTWARE OR THE USE OR OTHER DEALINGS IN
+#  THE SOFTWARE.
+
+module PhusionPassenger
+  module Rack
+    module Handler
+      def run(_app, options = {})
+        return if system(ruby_executable, '-S', find_passenger_standalone, 'start', *build_args(options))
+
+        raise 'Error starting Passenger'
+      end
+
+      def environment
+        ENV['RAILS_ENV'] || 'development'
+      end
+
+      def to_s
+        'Passenger application server'
+      end
+
+      private
+
+      def build_args(options)
+        args = ['-e', environment]
+        args << '-p' << options[:Port].to_s if options[:Port]
+        args << '-a' << options[:Host].to_s if options[:Host]
+        args << '-R' << options[:config].to_s if options[:config]
+        args
+      end
+
+      def rb_config
+        if defined?(::RbConfig)
+          ::RbConfig::CONFIG
+        else
+          ::Config::CONFIG
+        end
+      end
+
+      def ruby_executable
+        @ruby_executable ||= "#{rb_config['bindir']}/#{rb_config['RUBY_INSTALL_NAME']}#{rb_config['EXEEXT']}"
+      end
+
+      def find_passenger_standalone
+        ::File.join(::PhusionPassenger.bin_dir, 'passenger')
+      end
+    end
+  end
+end
diff --git a/src/ruby_supportlib/phusion_passenger/rack_handler.rb b/src/ruby_supportlib/phusion_passenger/rack_handler.rb
index 48c471a02b..f6132da4c5 100644
--- a/src/ruby_supportlib/phusion_passenger/rack_handler.rb
+++ b/src/ruby_supportlib/phusion_passenger/rack_handler.rb
@@ -1,3 +1,5 @@
+# frozen_string_literal: true
+
 #  Phusion Passenger - https://www.phusionpassenger.com/
 #  Copyright (c) 2016-2017 Phusion Holding B.V.
 #
@@ -27,76 +29,49 @@
 $LOAD_PATH.unshift(libdir)
 begin
   require 'rubygems'
+  require 'rackup'
 rescue LoadError
 end
 require 'phusion_passenger'
+require_relative 'rack/handler'
 ## Magic comment: end bootstrap ##
 
 PhusionPassenger.locate_directories
 
 require 'rbconfig'
 
-module Rack
-  module Handler
-    class PhusionPassenger
-      class << self
-        def run(app, options = {})
-          result = system(ruby_executable, '-S', find_passenger_standalone,
-            'start', *build_args(options))
-          if !result
-            raise "Error starting Passenger"
-          end
-        end
-
-        def environment
-          ENV['RAILS_ENV'] || 'development'
-        end
-
-        def to_s
-          'Passenger application server'
-        end
-
-      private
-        def build_args(options)
-          args = ['-e', environment]
-          if options[:Port]
-            args << '-p'
-            args << options[:Port].to_s
-          end
-          if options[:Host]
-            args << '-a'
-            args << options[:Host].to_s
-          end
-          if options[:config]
-            args << '-R'
-            args << options[:config].to_s
-          end
-          args
-        end
-
-        def rb_config
-          if defined?(::RbConfig)
-            ::RbConfig::CONFIG
-          else
-            ::Config::CONFIG
-          end
+# Rackup was removed in Rack 3, it is now a separate gem
+if Object.const_defined? :Rackup
+  module Rackup
+    module Handler
+      module PhusionPassenger
+        class << self
+          include ::PhusionPassenger::Rack::Handler
         end
+      end
 
-        def ruby_executable
-          @ruby_executable ||= rb_config['bindir'] + '/' +
-            rb_config['RUBY_INSTALL_NAME'] + rb_config['EXEEXT']
-        end
+      def self.default(options = {})
+        ::Rackup::Handler::PhusionPassenger
+      end
 
-        def find_passenger_standalone
-          ::File.join(::PhusionPassenger.bin_dir, 'passenger')
+      register :passenger, PhusionPassenger
+    end
+  end
+elsif Object.const_defined?(:Rack) && Rack.release < '3'
+  module Rack
+    module Handler
+      module PhusionPassenger
+        class << self
+          include ::PhusionPassenger::Rack::Handler
         end
       end
-    end
 
-    register 'passenger', 'Rack::Handler::PhusionPassenger'
-
-    def self.default(options = {})
-      Rack::Handler::PhusionPassenger
+      def self.default(options = {})
+        ::Rack::Handler::PhusionPassenger
+      end
     end
   end
+  ::Rack::Handler.register(:passenger, ::Rack::Handler::PhusionPassenger)
+else
+  raise 'Rack 3 must be used with the Rackup gem'
 end