diff --git a/changelog/fix_make_server_mode_aware_of_cache_root_directory.md b/changelog/fix_make_server_mode_aware_of_cache_root_directory.md
new file mode 100644
index 00000000000..cdc93c2cafd
--- /dev/null
+++ b/changelog/fix_make_server_mode_aware_of_cache_root_directory.md
@@ -0,0 +1 @@
+* [#10842](https://github.com/rubocop/rubocop/issues/10842): Make server mode aware of `CacheRootDirectory` config option value, `RUBOCOP_CACHE_ROOT`, and `XDG_CACHE_HOME` environment variables. ([@koic][])
diff --git a/lib/rubocop/cache_config.rb b/lib/rubocop/cache_config.rb
new file mode 100644
index 00000000000..504a32e8a19
--- /dev/null
+++ b/lib/rubocop/cache_config.rb
@@ -0,0 +1,29 @@
+# frozen_string_literal: true
+
+module RuboCop
+  # This class represents the cache config of the caching RuboCop runs.
+  # @api private
+  class CacheConfig
+    def self.root_dir
+      root = ENV.fetch('RUBOCOP_CACHE_ROOT', nil)
+      root ||= yield
+      root ||= if ENV.key?('XDG_CACHE_HOME')
+                 # Include user ID in the path to make sure the user has write
+                 # access.
+                 File.join(ENV.fetch('XDG_CACHE_HOME'), Process.uid.to_s)
+               else
+                 # On FreeBSD, the /home path is a symbolic link to /usr/home
+                 # and the $HOME environment variable returns the /home path.
+                 #
+                 # As $HOME is a built-in environment variable, FreeBSD users
+                 # always get a warning message.
+                 #
+                 # To avoid raising warn log messages on FreeBSD, we retrieve
+                 # the real path of the home folder.
+                 File.join(File.realpath(Dir.home), '.cache')
+               end
+
+      File.join(root, 'rubocop_cache')
+    end
+  end
+end
diff --git a/lib/rubocop/cli/command/auto_genenerate_config.rb b/lib/rubocop/cli/command/auto_genenerate_config.rb
index 73e9f34a0d2..420ca7bd99e 100644
--- a/lib/rubocop/cli/command/auto_genenerate_config.rb
+++ b/lib/rubocop/cli/command/auto_genenerate_config.rb
@@ -98,7 +98,7 @@ def execute_runner
         def add_inheritance_from_auto_generated_file(config_file)
           file_string = " #{relative_path_to_todo_from_options_config}"
 
-          config_file ||= ConfigLoader::DOTFILE
+          config_file ||= ConfigFinder::DOTFILE
 
           if File.exist?(config_file)
             files = Array(ConfigLoader.load_yaml_configuration(config_file)['inherit_from'])
@@ -113,7 +113,7 @@ def add_inheritance_from_auto_generated_file(config_file)
           write_config_file(config_file, file_string, rubocop_yml_contents)
 
           puts "Added inheritance from `#{relative_path_to_todo_from_options_config}` " \
-               "in `#{ConfigLoader::DOTFILE}`."
+               "in `#{ConfigFinder::DOTFILE}`."
         end
 
         def existing_configuration(config_file)
diff --git a/lib/rubocop/cli/command/init_dotfile.rb b/lib/rubocop/cli/command/init_dotfile.rb
index 0e85f48b8ae..dab89307fec 100644
--- a/lib/rubocop/cli/command/init_dotfile.rb
+++ b/lib/rubocop/cli/command/init_dotfile.rb
@@ -6,7 +6,7 @@ module Command
       # Generate a .rubocop.yml file in the current directory.
       # @api private
       class InitDotfile < Base
-        DOTFILE = ConfigLoader::DOTFILE
+        DOTFILE = ConfigFinder::DOTFILE
 
         self.command_name = :init
 
diff --git a/lib/rubocop/config_finder.rb b/lib/rubocop/config_finder.rb
new file mode 100644
index 00000000000..c990969f197
--- /dev/null
+++ b/lib/rubocop/config_finder.rb
@@ -0,0 +1,68 @@
+# frozen_string_literal: true
+
+require_relative 'file_finder'
+
+module RuboCop
+  # This class has methods related to finding configuration path.
+  # @api private
+  class ConfigFinder
+    DOTFILE = '.rubocop.yml'
+    XDG_CONFIG = 'config.yml'
+    RUBOCOP_HOME = File.realpath(File.join(File.dirname(__FILE__), '..', '..'))
+    DEFAULT_FILE = File.join(RUBOCOP_HOME, 'config', 'default.yml')
+
+    class << self
+      include FileFinder
+
+      attr_writer :project_root
+
+      def find_config_path(target_dir)
+        find_project_dotfile(target_dir) || find_user_dotfile || find_user_xdg_config ||
+          DEFAULT_FILE
+      end
+
+      # Returns the path RuboCop inferred as the root of the project. No file
+      # searches will go past this directory.
+      def project_root
+        @project_root ||= find_project_root
+      end
+
+      private
+
+      def find_project_root
+        pwd = Dir.pwd
+        gems_file = find_last_file_upwards('Gemfile', pwd) || find_last_file_upwards('gems.rb', pwd)
+        return unless gems_file
+
+        File.dirname(gems_file)
+      end
+
+      def find_project_dotfile(target_dir)
+        find_file_upwards(DOTFILE, target_dir, project_root)
+      end
+
+      def find_user_dotfile
+        return unless ENV.key?('HOME')
+
+        file = File.join(Dir.home, DOTFILE)
+
+        return file if File.exist?(file)
+      end
+
+      def find_user_xdg_config
+        xdg_config_home = expand_path(ENV.fetch('XDG_CONFIG_HOME', '~/.config'))
+        xdg_config = File.join(xdg_config_home, 'rubocop', XDG_CONFIG)
+
+        return xdg_config if File.exist?(xdg_config)
+      end
+
+      def expand_path(path)
+        File.expand_path(path)
+      rescue ArgumentError
+        # Could happen because HOME or ID could not be determined. Fall back on
+        # using the path literally in that case.
+        path
+      end
+    end
+  end
+end
diff --git a/lib/rubocop/config_loader.rb b/lib/rubocop/config_loader.rb
index f65356499f7..6bbcdcf3b16 100644
--- a/lib/rubocop/config_loader.rb
+++ b/lib/rubocop/config_loader.rb
@@ -3,6 +3,7 @@
 require 'erb'
 require 'yaml'
 require 'pathname'
+require_relative 'config_finder'
 
 module RuboCop
   # Raised when a RuboCop configuration file is not found.
@@ -15,8 +16,7 @@ class ConfigNotFoundError < Error
   # during a run of the rubocop program, if files in several
   # directories are inspected.
   class ConfigLoader
-    DOTFILE = '.rubocop.yml'
-    XDG_CONFIG = 'config.yml'
+    DOTFILE = ConfigFinder::DOTFILE
     RUBOCOP_HOME = File.realpath(File.join(File.dirname(__FILE__), '..', '..'))
     DEFAULT_FILE = File.join(RUBOCOP_HOME, 'config', 'default.yml')
 
@@ -25,7 +25,7 @@ class << self
 
       attr_accessor :debug, :ignore_parent_exclusion, :disable_pending_cops, :enable_pending_cops,
                     :ignore_unrecognized_cops
-      attr_writer :default_configuration, :project_root
+      attr_writer :default_configuration
       attr_reader :loaded_features
 
       alias debug? debug
@@ -95,8 +95,7 @@ def merge(base_hash, derived_hash)
       # user's home directory is checked. If there's no .rubocop.yml
       # there either, the path to the default file is returned.
       def configuration_file_for(target_dir)
-        find_project_dotfile(target_dir) || find_user_dotfile ||
-          find_user_xdg_config || DEFAULT_FILE
+        ConfigFinder.find_config_path(target_dir)
       end
 
       def configuration_from_file(config_file, check: true)
@@ -122,7 +121,7 @@ def possible_new_cops?(config)
       end
 
       def add_excludes_from_files(config, config_file)
-        exclusion_file = find_last_file_upwards(DOTFILE, config_file, project_root)
+        exclusion_file = find_last_file_upwards(DOTFILE, config_file, ConfigFinder.project_root)
 
         return unless exclusion_file
         return if PathUtil.relative_path(exclusion_file) == PathUtil.relative_path(config_file)
@@ -138,12 +137,6 @@ def default_configuration
         end
       end
 
-      # Returns the path RuboCop inferred as the root of the project. No file
-      # searches will go past this directory.
-      def project_root
-        @project_root ||= find_project_root
-      end
-
       PENDING_BANNER = <<~BANNER
         The following cops were added to RuboCop, but are not configured. Please set Enabled to either `true` or `false` in your `.rubocop.yml` file.
 
@@ -187,39 +180,6 @@ def file_path(file)
         File.absolute_path(file.is_a?(RemoteConfig) ? file.file : file)
       end
 
-      def find_project_dotfile(target_dir)
-        find_file_upwards(DOTFILE, target_dir, project_root)
-      end
-
-      def find_project_root
-        pwd = Dir.pwd
-        gems_file = find_last_file_upwards('Gemfile', pwd) || find_last_file_upwards('gems.rb', pwd)
-        return unless gems_file
-
-        File.dirname(gems_file)
-      end
-
-      def find_user_dotfile
-        return unless ENV.key?('HOME')
-
-        file = File.join(Dir.home, DOTFILE)
-        return file if File.exist?(file)
-      end
-
-      def find_user_xdg_config
-        xdg_config_home = expand_path(ENV.fetch('XDG_CONFIG_HOME', '~/.config'))
-        xdg_config = File.join(xdg_config_home, 'rubocop', XDG_CONFIG)
-        return xdg_config if File.exist?(xdg_config)
-      end
-
-      def expand_path(path)
-        File.expand_path(path)
-      rescue ArgumentError
-        # Could happen because HOME or ID could not be determined. Fall back on
-        # using the path literally in that case.
-        path
-      end
-
       def resolver
         @resolver ||= ConfigLoaderResolver.new
       end
diff --git a/lib/rubocop/result_cache.rb b/lib/rubocop/result_cache.rb
index 3a876f5d590..36dd86f3651 100644
--- a/lib/rubocop/result_cache.rb
+++ b/lib/rubocop/result_cache.rb
@@ -4,6 +4,7 @@
 require 'find'
 require 'etc'
 require 'zlib'
+require_relative 'cache_config'
 
 module RuboCop
   # Provides functionality for caching RuboCop runs.
@@ -67,24 +68,9 @@ def remove_files(files, dirs, remove_count)
     end
 
     def self.cache_root(config_store)
-      root = ENV.fetch('RUBOCOP_CACHE_ROOT', nil)
-      root ||= config_store.for_pwd.for_all_cops['CacheRootDirectory']
-      root ||= if ENV.key?('XDG_CACHE_HOME')
-                 # Include user ID in the path to make sure the user has write
-                 # access.
-                 File.join(ENV.fetch('XDG_CACHE_HOME'), Process.uid.to_s)
-               else
-                 # On FreeBSD, the /home path is a symbolic link to /usr/home
-                 # and the $HOME environment variable returns the /home path.
-                 #
-                 # As $HOME is a built-in environment variable, FreeBSD users
-                 # always get a warning message.
-                 #
-                 # To avoid raising warn log messages on FreeBSD, we retrieve
-                 # the real path of the home folder.
-                 File.join(File.realpath(Dir.home), '.cache')
-               end
-      File.join(root, 'rubocop_cache')
+      CacheConfig.root_dir do
+        config_store.for_pwd.for_all_cops['CacheRootDirectory']
+      end
     end
 
     def self.allow_symlinks_in_cache_location?(config_store)
diff --git a/lib/rubocop/server/cache.rb b/lib/rubocop/server/cache.rb
index e199b81f7f5..1f707466182 100644
--- a/lib/rubocop/server/cache.rb
+++ b/lib/rubocop/server/cache.rb
@@ -1,6 +1,8 @@
 # frozen_string_literal: true
 
 require 'pathname'
+require_relative '../cache_config'
+require_relative '../config_finder'
 
 #
 # This code is based on https://github.com/fohte/rubocop-daemon.
@@ -46,9 +48,32 @@ def dir
         end
 
         def cache_path
-          cache_root_dir = cache_root_path || File.join(Dir.home, '.cache')
+          cache_root_dir = if cache_root_path
+                             File.join(cache_root_path, 'rubocop_cache')
+                           else
+                             cache_root_dir_from_config
+                           end
 
-          File.expand_path(File.join(cache_root_dir, 'rubocop_cache', 'server'))
+          File.expand_path(File.join(cache_root_dir, 'server'))
+        end
+
+        def cache_root_dir_from_config
+          CacheConfig.root_dir do
+            # `RuboCop::ConfigStore` has heavy dependencies, this is a lightweight implementation
+            # so that only the necessary `CacheRootDirectory` can be obtained.
+            require 'yaml'
+
+            config_path = ConfigFinder.find_config_path(Dir.pwd)
+
+            # Ruby 3.1+
+            config_yaml = if Gem::Version.new(Psych::VERSION) >= Gem::Version.new('4.0.0')
+                            YAML.safe_load_file(config_path, permitted_classes: [Regexp, Symbol])
+                          else
+                            YAML.load_file(config_path)
+                          end
+
+            config_yaml.dig('AllCops', 'CacheRootDirectory')
+          end
         end
 
         def port_path
diff --git a/spec/rubocop/config_loader_spec.rb b/spec/rubocop/config_loader_spec.rb
index 3975d4335c3..199a1b34623 100644
--- a/spec/rubocop/config_loader_spec.rb
+++ b/spec/rubocop/config_loader_spec.rb
@@ -85,14 +85,14 @@
 
       before do
         # Force reload of project root
-        described_class.project_root = nil
+        RuboCop::ConfigFinder.project_root = nil
         create_empty_file('Gemfile')
         create_empty_file('../.rubocop.yml')
       end
 
       after do
         # Don't leak project root change
-        described_class.project_root = nil
+        RuboCop::ConfigFinder.project_root = nil
       end
 
       it 'ignores the spurious config and falls back to the provided default file if run from the project' do
diff --git a/spec/rubocop/cop/generator_spec.rb b/spec/rubocop/cop/generator_spec.rb
index 4d63cba18fc..f485b6f5146 100644
--- a/spec/rubocop/cop/generator_spec.rb
+++ b/spec/rubocop/cop/generator_spec.rb
@@ -352,7 +352,7 @@ def on_send(node)
 
     let(:config) do
       config = RuboCop::ConfigStore.new
-      path = File.join(RuboCop::ConfigLoader::RUBOCOP_HOME, RuboCop::ConfigLoader::DOTFILE)
+      path = File.join(RuboCop::ConfigLoader::RUBOCOP_HOME, RuboCop::ConfigFinder::DOTFILE)
       config.options_config = path
       config
     end
diff --git a/spec/rubocop/server/cache_spec.rb b/spec/rubocop/server/cache_spec.rb
index f146aeb5544..a10198168e6 100644
--- a/spec/rubocop/server/cache_spec.rb
+++ b/spec/rubocop/server/cache_spec.rb
@@ -3,6 +3,8 @@
 RSpec.describe RuboCop::Server::Cache do
   subject(:cache_class) { described_class }
 
+  include_context 'cli spec behavior'
+
   describe '.cache_path' do
     context 'when cache root path is not specified as default' do
       before do
@@ -27,5 +29,181 @@
         end
       end
     end
+
+    context 'when `CacheRootDirectory` configure value is set', :isolated_environment do
+      context 'when cache root path is not specified path' do
+        let(:cache_path) { File.join('/tmp/cache-root-directory', 'rubocop_cache', 'server') }
+
+        before do
+          cache_class.cache_root_path = nil
+        end
+
+        it 'contains the root from `CacheRootDirectory` configure value' do
+          create_file('.rubocop.yml', <<~YAML)
+            AllCops:
+              CacheRootDirectory: '/tmp/cache-root-directory'
+          YAML
+
+          if RuboCop::Platform.windows?
+            expect(cache_class.cache_path).to eq(cache_path.prepend('D:'))
+          else
+            expect(cache_class.cache_path).to eq(cache_path)
+          end
+        end
+      end
+
+      context 'when cache root path is not specified path and `XDG_CACHE_HOME` environment variable is spacified' do
+        let(:cache_path) { File.join('/tmp/cache-root-directory', 'rubocop_cache', 'server') }
+
+        around do |example|
+          cache_class.cache_root_path = nil
+
+          ENV['XDG_CACHE_HOME'] = '/tmp/cache-from-xdg-env'
+          begin
+            example.run
+          ensure
+            ENV.delete('XDG_CACHE_HOME')
+          end
+        end
+
+        it 'contains the root from `CacheRootDirectory` configure value' do
+          create_file('.rubocop.yml', <<~YAML)
+            AllCops:
+              CacheRootDirectory: '/tmp/cache-root-directory'
+          YAML
+
+          if RuboCop::Platform.windows?
+            expect(cache_class.cache_path).to eq(cache_path.prepend('D:'))
+          else
+            expect(cache_class.cache_path).to eq(cache_path)
+          end
+        end
+      end
+
+      context 'when cache root path is specified path' do
+        before do
+          cache_class.cache_root_path = '/tmp'
+        end
+
+        it 'contains the root from cache root path' do
+          create_file('.rubocop.yml', <<~YAML)
+            AllCops:
+              CacheRootDirectory: '/tmp/cache-root-directory'
+          YAML
+
+          if RuboCop::Platform.windows?
+            expect(cache_class.cache_path).to eq(File.join('D:/tmp', 'rubocop_cache', 'server'))
+          else
+            expect(cache_class.cache_path).to eq(File.join('/tmp', 'rubocop_cache', 'server'))
+          end
+        end
+      end
+    end
+
+    context 'when `RUBOCOP_CACHE_ROOT` environment variable is set' do
+      around do |example|
+        ENV['RUBOCOP_CACHE_ROOT'] = '/tmp/rubocop-cache-root-env'
+        begin
+          example.run
+        ensure
+          ENV.delete('RUBOCOP_CACHE_ROOT')
+        end
+      end
+
+      context 'when cache root path is not specified path' do
+        let(:cache_path) { File.join('/tmp/rubocop-cache-root-env', 'rubocop_cache', 'server') }
+
+        before do
+          cache_class.cache_root_path = nil
+        end
+
+        it 'contains the root from `RUBOCOP_CACHE_ROOT`' do
+          if RuboCop::Platform.windows?
+            expect(cache_class.cache_path).to eq(cache_path.prepend('D:'))
+          else
+            expect(cache_class.cache_path).to eq(cache_path)
+          end
+        end
+      end
+
+      context 'when cache root path is not specified path and `XDG_CACHE_HOME` environment variable is specified' do
+        let(:cache_path) { File.join('/tmp/rubocop-cache-root-env', 'rubocop_cache', 'server') }
+
+        around do |example|
+          cache_class.cache_root_path = nil
+
+          ENV['XDG_CACHE_HOME'] = '/tmp/cache-from-xdg-env'
+          begin
+            example.run
+          ensure
+            ENV.delete('XDG_CACHE_HOME')
+          end
+        end
+
+        it 'contains the root from `RUBOCOP_CACHE_ROOT`' do
+          if RuboCop::Platform.windows?
+            expect(cache_class.cache_path).to eq(cache_path.prepend('D:'))
+          else
+            expect(cache_class.cache_path).to eq(cache_path)
+          end
+        end
+      end
+
+      context 'when cache root path is specified path' do
+        before do
+          cache_class.cache_root_path = '/tmp'
+        end
+
+        it 'contains the root from cache root path' do
+          if RuboCop::Platform.windows?
+            expect(cache_class.cache_path).to eq(File.join('D:/tmp', 'rubocop_cache', 'server'))
+          else
+            expect(cache_class.cache_path).to eq(File.join('/tmp', 'rubocop_cache', 'server'))
+          end
+        end
+      end
+    end
+
+    context 'when `XDG_CACHE_HOME` environment variable is set' do
+      around do |example|
+        ENV['XDG_CACHE_HOME'] = '/tmp/cache-from-xdg-env'
+        begin
+          example.run
+        ensure
+          ENV.delete('XDG_CACHE_HOME')
+        end
+      end
+
+      context 'when cache root path is not specified path' do
+        let(:puid) { Process.uid.to_s }
+        let(:cache_path) { File.join('/tmp/cache-from-xdg-env', puid, 'rubocop_cache', 'server') }
+
+        before do
+          cache_class.cache_root_path = nil
+        end
+
+        it 'contains the root from `XDG_CACHE_HOME`' do
+          if RuboCop::Platform.windows?
+            expect(cache_class.cache_path).to eq(cache_path.prepend('D:'))
+          else
+            expect(cache_class.cache_path).to eq(cache_path)
+          end
+        end
+      end
+
+      context 'when cache root path is specified path' do
+        before do
+          cache_class.cache_root_path = '/tmp'
+        end
+
+        it 'contains the root from cache root path' do
+          if RuboCop::Platform.windows?
+            expect(cache_class.cache_path).to eq(File.join('D:/tmp', 'rubocop_cache', 'server'))
+          else
+            expect(cache_class.cache_path).to eq(File.join('/tmp', 'rubocop_cache', 'server'))
+          end
+        end
+      end
+    end
   end
 end