diff --git a/actionpack/lib/action_dispatch/system_test_case.rb b/actionpack/lib/action_dispatch/system_test_case.rb
index 3e969abcb94f..d19dadb90cc2 100644
--- a/actionpack/lib/action_dispatch/system_test_case.rb
+++ b/actionpack/lib/action_dispatch/system_test_case.rb
@@ -159,7 +159,7 @@ def self.driven_by(driver, using: :chrome, screen_size: [1400, 1400], options: {
       self.driver = SystemTesting::Driver.new(driver, **driver_options, &capabilities)
     end
 
-    # Configuration for the System Test application server
+    # Configuration for the System Test application server.
     #
     # By default this is localhost. This method allows the host and port to be specified manually.
     def self.served_by(host:, port:)
diff --git a/railties/CHANGELOG.md b/railties/CHANGELOG.md
index 54f44fb57ab3..1fbf1bae7782 100644
--- a/railties/CHANGELOG.md
+++ b/railties/CHANGELOG.md
@@ -1,3 +1,19 @@
+*   Generate a .devcontainer folder and its contents when creating a new app.
+
+    The .devcontainer folder includes everything needed to boot the app and do development in a remote container.
+
+    The container setup includes:
+     - A redis container for Sidekiq and Action Cable
+     - A database (SQLite, Postgres, MySQL or MariaDB)
+     - A Headless chrome container for system tests
+     - Active Storage configured to use the local disk and with preview features working
+
+    If any of these options are skipped in the app setup they will not be included in the container configuration.
+
+    These files can be skipped using the `--skip-devcontainer` option.
+
+    *Andrew Novoselac & Rafael Mendonça França*
+
 *   Introduce `SystemTestCase#servered_by` for configuring the System Test application server
 
     By default this is localhost. This method allows the host and port to be specified manually.
diff --git a/railties/lib/rails/generators/app_base.rb b/railties/lib/rails/generators/app_base.rb
index 9116579ad0a5..d7f044c7bdcf 100644
--- a/railties/lib/rails/generators/app_base.rb
+++ b/railties/lib/rails/generators/app_base.rb
@@ -109,6 +109,9 @@ def self.add_shared_options_for(name)
         class_option :skip_ci,             type: :boolean, default: nil,
                                            desc: "Skip GitHub CI files"
 
+        class_option :skip_devcontainer,   type: :boolean, default: nil,
+                                           desc: "Skip devcontainer files"
+
         class_option :dev,                 type: :boolean, default: nil,
                                            desc: "Set up the #{name} with Gemfile pointing to your Rails checkout"
 
@@ -400,6 +403,10 @@ def skip_ci?
         options[:skip_ci]
       end
 
+      def skip_devcontainer?
+        options[:skip_devcontainer]
+      end
+
       class GemfileEntry < Struct.new(:name, :version, :comment, :options, :commented_out)
         def initialize(name, version, comment, options = {}, commented_out = false)
           super
diff --git a/railties/lib/rails/generators/rails/app/app_generator.rb b/railties/lib/rails/generators/rails/app/app_generator.rb
index 51f08464ba55..33e9a29ff251 100644
--- a/railties/lib/rails/generators/rails/app/app_generator.rb
+++ b/railties/lib/rails/generators/rails/app/app_generator.rb
@@ -266,6 +266,14 @@ def vendor
     def config_target_version
       @config_target_version || Rails::VERSION::STRING.to_f
     end
+
+    def devcontainer
+      empty_directory ".devcontainer"
+
+      template ".devcontainer/devcontainer.json"
+      template ".devcontainer/Dockerfile"
+      template ".devcontainer/docker-compose.yml"
+    end
   end
 
   module Generators
@@ -455,6 +463,11 @@ def create_storage_files
         build(:storage)
       end
 
+      def create_devcontainer_files
+        return if skip_devcontainer? || options[:dummy_app]
+        build(:devcontainer)
+      end
+
       def delete_app_assets_if_api_option
         if options[:api]
           remove_dir "app/assets"
@@ -592,6 +605,44 @@ def after_bundle(&block) # :doc:
       def get_builder_class
         defined?(::AppBuilder) ? ::AppBuilder : Rails::AppBuilder
       end
+
+      def devcontainer_dependencies
+        return @devcontainer_dependencies if @devcontainer_dependencies
+
+        @devcontainer_dependencies = []
+
+        @devcontainer_dependencies << "selenium" if depends_on_system_test?
+        @devcontainer_dependencies << "redis" unless options.skip_action_cable? && options.skip_active_job?
+        @devcontainer_dependencies << "postgres" if options.database == "postgresql"
+        @devcontainer_dependencies << "mysql" if options.database == "mysql"
+        @devcontainer_dependencies << "mariadb" if options.database == "trilogy"
+
+        @devcontainer_dependencies
+      end
+
+      def devcontainer_variables
+        return @devcontainer_variables if @devcontainer_variables
+
+        @devcontainer_variables = {}
+
+        @devcontainer_variables["CAPYBARA_SERVER_PORT"] = "45678" if depends_on_system_test?
+        @devcontainer_variables["SELENIUM_HOST"] = "selenium" if depends_on_system_test?
+        @devcontainer_variables["JOBS_REDIS_URL"] = "redis://redis:6379/1" unless options.skip_active_job?
+        @devcontainer_variables["CABLE_REDIS_URL"] = "redis://redis:6379/1" unless options.skip_action_cable?
+        @devcontainer_variables["RAILS_DATABASE_HOST"] = "postgres" if options.database == "postgresql"
+        @devcontainer_variables["RAILS_DATABASE_HOST"] = "mysql" if options.database == "mysql"
+        @devcontainer_variables["RAILS_DATABASE_HOST"] = "mariadb" if options.database == "trilogy"
+
+        @devcontainer_variables
+      end
+
+      def mysql_database_host
+        if skip_devcontainer?
+          "localhost"
+        else
+          "<%= ENV.fetch(\"RAILS_DATABASE_HOST\") { \"localhost\" } %>"
+        end
+      end
     end
 
     # This class handles preparation of the arguments before the AppGenerator is
diff --git a/railties/lib/rails/generators/rails/app/templates/.devcontainer/Dockerfile.tt b/railties/lib/rails/generators/rails/app/templates/.devcontainer/Dockerfile.tt
new file mode 100644
index 000000000000..e8368c6ab30c
--- /dev/null
+++ b/railties/lib/rails/generators/rails/app/templates/.devcontainer/Dockerfile.tt
@@ -0,0 +1,14 @@
+FROM mcr.microsoft.com/devcontainers/ruby:1-3-bookworm
+
+<%- unless options.skip_active_storage -%>
+# Install packages needed to build gems
+RUN apt-get update -qq && \
+    apt-get install --no-install-recommends -y \
+      libvips \
+      #  For video thumbnails
+      ffmpeg \
+      # For pdf thumbnails. If you want to use mupdf instead of poppler,
+      # you can install the following packages instead:
+      # mupdf mupdf-tools
+      poppler-utils
+<%- end -%>
\ No newline at end of file
diff --git a/railties/lib/rails/generators/rails/app/templates/.devcontainer/devcontainer.json.tt b/railties/lib/rails/generators/rails/app/templates/.devcontainer/devcontainer.json.tt
new file mode 100644
index 000000000000..6aae049fa72d
--- /dev/null
+++ b/railties/lib/rails/generators/rails/app/templates/.devcontainer/devcontainer.json.tt
@@ -0,0 +1,34 @@
+// For format details, see https://aka.ms/devcontainer.json. For config options, see the
+// README at: https://github.com/devcontainers/templates/tree/main/src/ruby
+{
+  "name": "<%= app_name %>",
+  "dockerComposeFile": "docker-compose.yml",
+  "service": "rails-app",
+  "workspaceFolder": "/workspaces/${localWorkspaceFolderBasename}",
+
+  // Features to add to the dev container. More info: https://containers.dev/features.
+  "features": {
+    "ghcr.io/devcontainers/features/github-cli:1": {}
+  },
+
+<%- if !devcontainer_variables.empty? -%>
+  "containerEnv": {
+    <%= devcontainer_variables.map { |key, value| "\"#{key}\": \"#{value}\"" }.join(",\n    ") %>
+  },
+<%- end -%>
+
+  // Features to add to the dev container. More info: https://containers.dev/features.
+  // "features": {},
+
+  // Use 'forwardPorts' to make a list of ports inside the container available locally.
+  // "forwardPorts": [],
+
+  // Configure tool-specific properties.
+  // "customizations": {},
+
+  // Uncomment to connect as root instead. More info: https://aka.ms/dev-containers-non-root.
+  // "remoteUser": "root",
+
+  // Use 'postCreateCommand' to run commands after the container is created.
+  "postCreateCommand": "bin/setup"
+}
diff --git a/railties/lib/rails/generators/rails/app/templates/.devcontainer/docker-compose.yml.tt b/railties/lib/rails/generators/rails/app/templates/.devcontainer/docker-compose.yml.tt
new file mode 100644
index 000000000000..a785fb1557c5
--- /dev/null
+++ b/railties/lib/rails/generators/rails/app/templates/.devcontainer/docker-compose.yml.tt
@@ -0,0 +1,78 @@
+services:
+  rails-app:
+    build:
+      context: ..
+      dockerfile: .devcontainer/Dockerfile
+
+    volumes:
+      - ../..:/workspaces:cached
+
+    # Overrides default command so things don't shut down after the process ends.
+    command: sleep infinity
+
+    networks:
+      - default
+
+    # Uncomment the next line to use a non-root user for all processes.
+    # user: vscode
+
+    # Use "forwardPorts" in **devcontainer.json** to forward an app port locally.
+    # (Adding the "ports" property to this file will not forward from a Codespace.)
+    ports:
+      - 45678:45678
+<%- if !devcontainer_dependencies.empty? -%>
+    depends_on:
+<%- devcontainer_dependencies.each do |dependency| -%>
+      - <%= dependency %>
+<%- end -%>
+<%- end -%>
+
+<%- if depends_on_system_test? -%>
+  selenium:
+    image: seleniarm/standalone-chromium
+    restart: unless-stopped
+    networks:
+      - default
+<%- end -%>
+
+<%- unless options.skip_active_job? && options.skip_action_cable? -%>
+  redis:
+    image: redis:7.2
+    restart: unless-stopped
+    networks:
+      - default
+    ports:
+      - 6379:6379
+<%- end -%>
+
+<%- if options.database == "postgresql" -%>
+  postgres:
+    image: postgres:16.1
+    restart: unless-stopped
+    networks:
+      - default
+    environment:
+      POSTGRES_USER: postgres
+      POSTGRES_PASSWORD: postgres
+<%- end -%>
+
+<%- if options.database == "mysql" -%>
+  mysql:
+    image: mysql/mysql-server:8.0
+    restart: unless-stopped
+    environment:
+      MYSQL_ALLOW_EMPTY_PASSWORD: true
+      MYSQL_ROOT_HOST: "%"
+    networks:
+      - default
+<%- end -%>
+
+<%- if options.database == "trilogy" -%>
+  mariadb:
+    image: mariadb:10.5
+    restart: unless-stopped
+    networks:
+      - default
+    environment:
+      MARIADB_ALLOW_EMPTY_ROOT_PASSWORD: true
+<%- end -%>
\ No newline at end of file
diff --git a/railties/lib/rails/generators/rails/app/templates/config/databases/mysql.yml.tt b/railties/lib/rails/generators/rails/app/templates/config/databases/mysql.yml.tt
index e3c5f28566ab..ee6940810711 100644
--- a/railties/lib/rails/generators/rails/app/templates/config/databases/mysql.yml.tt
+++ b/railties/lib/rails/generators/rails/app/templates/config/databases/mysql.yml.tt
@@ -18,7 +18,7 @@ default: &default
 <% if mysql_socket -%>
   socket: <%= mysql_socket %>
 <% else -%>
-  host: <%%= ENV.fetch("RAILS_DATABASE_HOST") { "localhost" } %>
+  host: <%= mysql_database_host %>
 <% end -%>
 
 development:
diff --git a/railties/lib/rails/generators/rails/app/templates/config/databases/postgresql.yml.tt b/railties/lib/rails/generators/rails/app/templates/config/databases/postgresql.yml.tt
index d58a81e7f5b0..b4bbe90690d1 100644
--- a/railties/lib/rails/generators/rails/app/templates/config/databases/postgresql.yml.tt
+++ b/railties/lib/rails/generators/rails/app/templates/config/databases/postgresql.yml.tt
@@ -18,11 +18,13 @@ default: &default
   # For details on connection pooling, see Rails configuration guide
   # https://guides.rubyonrails.org/configuring.html#database-pooling
   pool: <%%= ENV.fetch("RAILS_MAX_THREADS") { 5 } %>
+<% unless skip_devcontainer? -%>
   <%% if ENV["RAILS_DATABASE_HOST"] %>
   host: <%%= ENV["RAILS_DATABASE_HOST"] %>
   username: postgres
   password: postgres
   <%% end %>
+<% end %>
 
 development:
   <<: *default
diff --git a/railties/lib/rails/generators/rails/app/templates/config/databases/trilogy.yml.tt b/railties/lib/rails/generators/rails/app/templates/config/databases/trilogy.yml.tt
index 33e790ae42c2..b0cd1e73f9cc 100644
--- a/railties/lib/rails/generators/rails/app/templates/config/databases/trilogy.yml.tt
+++ b/railties/lib/rails/generators/rails/app/templates/config/databases/trilogy.yml.tt
@@ -18,7 +18,7 @@ default: &default
 <% if mysql_socket -%>
   socket: <%= mysql_socket %>
 <% else -%>
-  host: <%%= ENV.fetch("RAILS_DATABASE_HOST") { "localhost" } %>
+  host: <%= mysql_database_host %>
 <% end -%>
 
 development:
diff --git a/railties/lib/rails/generators/rails/app/templates/test/application_system_test_case.rb.tt b/railties/lib/rails/generators/rails/app/templates/test/application_system_test_case.rb.tt
index cee29fd2143e..b5e2a0b0a98c 100644
--- a/railties/lib/rails/generators/rails/app/templates/test/application_system_test_case.rb.tt
+++ b/railties/lib/rails/generators/rails/app/templates/test/application_system_test_case.rb.tt
@@ -1,5 +1,18 @@
 require "test_helper"
 
 class ApplicationSystemTestCase < ActionDispatch::SystemTestCase
+<% if skip_devcontainer? -%>
   driven_by :selenium, using: :headless_chrome, screen_size: [ 1400, 1400 ]
+<% else -%>
+  if ENV["CAPYBARA_SERVER_PORT"]
+    served_by host: "rails-app", port: ENV["CAPYBARA_SERVER_PORT"]
+
+    driven_by :selenium, using: :headless_chrome, screen_size: [ 1400, 1400 ], options: {
+      browser: :remote,
+      url: "http://#{ENV["SELENIUM_HOST"]}:4444",
+    }
+  else
+    driven_by :selenium, using: :headless_chrome, screen_size: [ 1400, 1400 ]
+  end
+<% end -%>
 end
diff --git a/railties/test/generators/app_generator_test.rb b/railties/test/generators/app_generator_test.rb
index dd7742d5d0fb..fe4efb8b0191 100644
--- a/railties/test/generators/app_generator_test.rb
+++ b/railties/test/generators/app_generator_test.rb
@@ -5,6 +5,9 @@
 require "generators/shared_generator_tests"
 
 DEFAULT_APP_FILES = %w(
+  .devcontainer/Dockerfile
+  .devcontainer/devcontainer.json
+  .devcontainer/docker-compose.yml
   .dockerignore
   .git
   .gitattributes
@@ -1229,6 +1232,136 @@ def test_name_option
     assert_file "config/application.rb", /^module MyApp$/
   end
 
+  def test_devcontainer
+    run_generator [destination_root, "--name=my-app"]
+
+    assert_file(".devcontainer/devcontainer.json") do |content|
+      assert_match(/"name": "my_app"/, content)
+      assert_match(/"JOBS_REDIS_URL": "redis:\/\/redis:6379\/1"/, content)
+      assert_match(/"CABLE_REDIS_URL": "redis:\/\/redis:6379\/1"/, content)
+      assert_match(/"CAPYBARA_SERVER_PORT": "45678"/, content)
+      assert_match(/"SELENIUM_HOST": "selenium"/, content)
+    end
+    assert_file(".devcontainer/Dockerfile") do |content|
+      assert_match(/libvips/, content)
+      assert_match(/ffmpeg/, content)
+      assert_match(/poppler-utils/, content)
+    end
+    assert_file(".devcontainer/docker-compose.yml") do |content|
+      assert_match(/depends_on:/, content)
+      assert_match(/- selenium/, content)
+      assert_match(/- redis/, content)
+      assert_no_match(/- maria_db/, content)
+      assert_no_match(/- postgres/, content)
+      assert_no_match(/- mysql/, content)
+
+      assert_match(/selenium:/, content)
+      assert_match(/redis:/, content)
+      assert_no_match(/maria_db:/, content)
+      assert_no_match(/postgres:/, content)
+      assert_no_match(/mysql:/, content)
+    end
+  end
+
+  def test_devcontainer_no_redis_skipping_action_cable_and_active_job
+    run_generator [ destination_root, "--skip_action_cable", "--skip_active_job" ]
+
+    assert_file(".devcontainer/docker-compose.yml") do |content|
+      assert_no_match(/- redis/, content)
+      assert_no_match(/redis:/, content)
+    end
+  end
+
+  def test_devcontainer_no_jobs_redis_url_when_skipping_active_job
+    run_generator [ destination_root, "--skip_active_job" ]
+
+    assert_file(".devcontainer/devcontainer.json") do |content|
+      assert_no_match(/JOBS_REDIS_URL/, content)
+    end
+  end
+
+  def test_devcontainer_no_cable_redis_url_when_skipping_action_cable
+    run_generator [ destination_root, "--skip_action_cable" ]
+
+    assert_file(".devcontainer/devcontainer.json") do |content|
+      assert_no_match(/CABLE_REDIS_URL/, content)
+    end
+  end
+
+  def test_devonctainer_postgresql
+    run_generator [ destination_root, "-d", "postgresql" ]
+
+    assert_file(".devcontainer/docker-compose.yml") do |content|
+      assert_match(/- postgres/, content)
+      assert_match(/postgres:/, content)
+    end
+    assert_file(".devcontainer/devcontainer.json") do |content|
+      assert_match(/"RAILS_DATABASE_HOST": "postgres"/, content)
+    end
+  end
+
+  def test_devonctainer_mysql
+    run_generator [ destination_root, "-d", "mysql" ]
+
+    assert_file(".devcontainer/docker-compose.yml") do |content|
+      assert_match(/- mysql/, content)
+      assert_match(/mysql:/, content)
+    end
+    assert_file(".devcontainer/devcontainer.json") do |content|
+      assert_match(/"RAILS_DATABASE_HOST": "mysql"/, content)
+    end
+  end
+
+  def test_devonctainer_mariadb
+    run_generator [ destination_root, "-d", "trilogy" ]
+
+    assert_file(".devcontainer/docker-compose.yml") do |content|
+      assert_match(/- mariadb/, content)
+      assert_match(/mariadb:/, content)
+    end
+    assert_file(".devcontainer/devcontainer.json") do |content|
+      assert_match(/"RAILS_DATABASE_HOST": "mariadb"/, content)
+    end
+  end
+
+  def test_devcontainer_no_selenium_when_skipping_system_test
+    run_generator [ destination_root, "--skip_system_test" ]
+
+    assert_file(".devcontainer/docker-compose.yml") do |content|
+      assert_no_match(/- selenium/, content)
+      assert_no_match(/selenium:/, content)
+    end
+    assert_file(".devcontainer/devcontainer.json") do |content|
+      assert_no_match(/CAPYBARA_SERVER_PORT/, content)
+    end
+  end
+
+  def test_devcontainer_no_Dockerfile_packages_when_skipping_active_storage
+    run_generator [ destination_root, "--skip_active_storage" ]
+
+    assert_file(".devcontainer/Dockerfile") do |content|
+      assert_no_match(/libvips/, content)
+      assert_no_match(/ffmpeg/, content)
+      assert_no_match(/poppler-utils/, content)
+    end
+  end
+
+  def test_devcontainer_no_depends_on_when_no_dependencies
+    run_generator [ destination_root, "--minimal" ]
+
+    assert_file(".devcontainer/docker-compose.yml") do |content|
+      assert_no_match(/depends_on:/, content)
+    end
+  end
+
+  def test_skip_devcontainer
+    run_generator [ destination_root, "--skip_devcontainer" ]
+
+    assert_no_file(".devcontainer/devcontainer.json")
+    assert_no_file(".devcontainer/Dockerfile")
+    assert_no_file(".devcontainer/docker-compose.yml")
+  end
+
   private
     def assert_node_files
       assert_file ".node-version" do |content|