diff --git a/railties/CHANGELOG.md b/railties/CHANGELOG.md
index 8b8956a6b3bcd..f26546b5e4b40 100644
--- a/railties/CHANGELOG.md
+++ b/railties/CHANGELOG.md
@@ -1,3 +1,9 @@
+## Unreleased
+
+*   Fix a regression in which autoload paths were initialized too late.
+
+    *Xavier Noria*
+
 ## Rails 7.0.0.alpha2 (September 15, 2021) ##
 
 *   Fix activestorage dependency in the npm package.
diff --git a/railties/lib/rails/application/bootstrap.rb b/railties/lib/rails/application/bootstrap.rb
index 6791992dacf82..44ccef5cea4cf 100644
--- a/railties/lib/rails/application/bootstrap.rb
+++ b/railties/lib/rails/application/bootstrap.rb
@@ -66,7 +66,7 @@ module Bootstrap
 
       # We setup the once autoloader this early so that engines and applications
       # are able to autoload from these paths during initialization.
-      initializer :setup_once_autoloader do
+      initializer :setup_once_autoloader, after: :set_eager_load_paths, before: :bootstrap_hook do
         autoloader = Rails.autoloaders.once
 
         ActiveSupport::Dependencies.autoload_once_paths.freeze
diff --git a/railties/lib/rails/engine.rb b/railties/lib/rails/engine.rb
index ce3f745539e2e..1849638323f37 100644
--- a/railties/lib/rails/engine.rb
+++ b/railties/lib/rails/engine.rb
@@ -570,14 +570,12 @@ def load_seed
       $LOAD_PATH.uniq!
     end
 
-    initializer :set_autoload_once_paths, before: :setup_once_autoloader do
-      config.autoload_once_paths.freeze
+    initializer :set_autoload_paths, before: :bootstrap_hook do
+      ActiveSupport::Dependencies.autoload_paths.unshift(*_all_autoload_paths)
       ActiveSupport::Dependencies.autoload_once_paths.unshift(*_all_autoload_once_paths)
-    end
 
-    initializer :set_autoload_paths, before: :setup_main_autoloader do
       config.autoload_paths.freeze
-      ActiveSupport::Dependencies.autoload_paths.unshift(*_all_autoload_paths)
+      config.autoload_once_paths.freeze
     end
 
     initializer :set_eager_load_paths, before: :bootstrap_hook do
diff --git a/railties/test/railties/engine_test.rb b/railties/test/railties/engine_test.rb
index 42b956b7c831d..432eed4e67f1e 100644
--- a/railties/test/railties/engine_test.rb
+++ b/railties/test/railties/engine_test.rb
@@ -233,6 +233,26 @@ class AddFirstNameToUsers < ActiveRecord::Migration::Current
       assert_equal "Another", Another.name
     end
 
+    test "when the bootstrap hook runs, autoload paths are set" do
+      $test_autoload_once_paths = []
+      $test_autoload_paths = []
+
+      add_to_config <<~RUBY
+        # Unrealistic configuration, but keeps the test simple.
+        config.autoload_once_paths << "#{app_path}/app/helpers"
+
+        initializer "inspect autoload paths", after: :bootstrap_hook do
+          $test_autoload_once_paths += ActiveSupport::Dependencies.autoload_once_paths
+          $test_autoload_paths += ActiveSupport::Dependencies.autoload_paths
+        end
+      RUBY
+
+      boot_rails
+
+      assert_includes $test_autoload_once_paths, "#{app_path}/app/helpers"
+      assert_includes $test_autoload_paths, "#{app_path}/app/controllers"
+    end
+
     test "puts its models directory on autoload path" do
       @plugin.write "app/models/my_bukkit.rb", "class MyBukkit ; end"
       boot_rails