diff --git a/ee/lib/remote_development/messages.rb b/ee/lib/remote_development/messages.rb
index 14ab0d9d366bb2493b597296d2a8859e26c177d2..d998d0742a5b1da3e9a4b0566d24f0264f57c2c4 100644
--- a/ee/lib/remote_development/messages.rb
+++ b/ee/lib/remote_development/messages.rb
@@ -37,9 +37,10 @@ module Messages
     WorkspaceReconcileParamsValidationFailed = Class.new(Message)
 
     # Settings errors
-    SettingsEnvironmentVariableReadFailed = Class.new(Message)
     SettingsCurrentSettingsReadFailed = Class.new(Message)
+    SettingsEnvironmentVariableReadFailed = Class.new(Message)
     SettingsVscodeExtensionsGalleryValidationFailed = Class.new(Message)
+    SettingsVscodeExtensionsGalleryMetadataValidationFailed = Class.new(Message)
 
     # Namespace Cluster Agent Mapping create errors
     NamespaceClusterAgentMappingAlreadyExists = Class.new(Message)
diff --git a/ee/lib/remote_development/settings/defaults_initializer.rb b/ee/lib/remote_development/settings/defaults_initializer.rb
index 9d4397bc6cbeb43892389ae0a28df7f9f62e047a..c04f001d949c14104df35d91452f02d3688a2119 100644
--- a/ee/lib/remote_development/settings/defaults_initializer.rb
+++ b/ee/lib/remote_development/settings/defaults_initializer.rb
@@ -29,6 +29,10 @@ def self.default_settings
               resource_url_template: "https://open-vsx.org/api/{publisher}/{name}/{version}/file/{path}"
             },
             Hash
+          ],
+          vscode_extensions_gallery_metadata: [
+            {}, # NOTE: There is no default, the value is always generated by ExtensionsGalleryMetadataGenerator
+            Hash
           ]
         }
       end
diff --git a/ee/lib/remote_development/settings/extensions_gallery_metadata_generator.rb b/ee/lib/remote_development/settings/extensions_gallery_metadata_generator.rb
new file mode 100644
index 0000000000000000000000000000000000000000..4cb20daabbc6e1fe5e9f8f1e1bd9019232dae990
--- /dev/null
+++ b/ee/lib/remote_development/settings/extensions_gallery_metadata_generator.rb
@@ -0,0 +1,66 @@
+# frozen_string_literal: true
+
+module RemoteDevelopment
+  module Settings
+    class ExtensionsGalleryMetadataGenerator
+      include Messages
+
+      # NOTE: These `disabled_reason` enumeration values are also referenced/consumed in
+      #       the "gitlab-web-ide" and "gitlab-web-ide-vscode-fork" projects
+      #       (https://gitlab.com/gitlab-org/gitlab-web-ide & https://gitlab.com/gitlab-org/gitlab-web-ide-vscode-fork),
+      #       so we must ensure that any changes made here are also reflected in those projects.
+      DISABLED_REASONS =
+        %i[
+          no_user
+          no_flag
+          instance_disabled
+          opt_in_unset
+          opt_in_disabled
+        ].to_h { |reason| [reason, reason] }.freeze
+
+      # @param [Hash] value
+      # @return [Hash]
+      def self.generate(value)
+        value => { options: Hash => options }
+        options_with_defaults = { user: nil, vscode_extensions_marketplace_feature_flag_enabled: nil }.merge(options)
+        options_with_defaults => {
+          user: ::User | NilClass => user,
+          vscode_extensions_marketplace_feature_flag_enabled: TrueClass | FalseClass | NilClass =>
+            extensions_marketplace_feature_flag_enabled
+        }
+
+        extensions_gallery_metadata = generate_settings(
+          user: user,
+          flag_enabled: extensions_marketplace_feature_flag_enabled
+        )
+
+        value[:settings][:vscode_extensions_gallery_metadata] = extensions_gallery_metadata
+        value
+      end
+
+      # @param [User, nil] user
+      # @param [Boolean, nil] flag_enabled
+      # @return [Hash]
+      def self.generate_settings(user:, flag_enabled:)
+        return { enabled: false, disabled_reason: DISABLED_REASONS.fetch(:no_user) } unless user
+        return { enabled: false, disabled_reason: DISABLED_REASONS.fetch(:no_flag) } if flag_enabled.nil?
+        return { enabled: false, disabled_reason: DISABLED_REASONS.fetch(:instance_disabled) } unless flag_enabled
+
+        # noinspection RubyNilAnalysis -- RubyMine doesn't realize user can't be nil because of guard clause above
+        opt_in_status = user.extensions_marketplace_opt_in_status.to_sym
+
+        return { enabled: true } if opt_in_status == :enabled
+        return { enabled: false, disabled_reason: DISABLED_REASONS.fetch(:opt_in_unset) } if opt_in_status == :unset
+
+        if opt_in_status == :disabled
+          return { enabled: false, disabled_reason: DISABLED_REASONS.fetch(:opt_in_disabled) }
+        end
+
+        # This is an internal bug due to an enumeration mismatch/inconsistency with the model, so lets throw an
+        # exception up the stack and let it be returned as a 500 - don't try to handle it via the ROP chain
+        raise "Invalid user.extensions_marketplace_opt_in_status: '#{opt_in_status}'. " \
+          "Supported statuses are: #{Enums::WebIde::ExtensionsMarketplaceOptInStatus.statuses.keys}." # rubocop:disable Layout/LineEndStringConcatenationIndentation -- This is already changed in the next version of gitlab-styles
+      end
+    end
+  end
+end
diff --git a/ee/lib/remote_development/settings/extensions_gallery_metadata_validator.rb b/ee/lib/remote_development/settings/extensions_gallery_metadata_validator.rb
new file mode 100644
index 0000000000000000000000000000000000000000..5434d5617b6a4880ca32819217ea53f52022e79f
--- /dev/null
+++ b/ee/lib/remote_development/settings/extensions_gallery_metadata_validator.rb
@@ -0,0 +1,80 @@
+# frozen_string_literal: true
+
+module RemoteDevelopment
+  module Settings
+    class ExtensionsGalleryMetadataValidator
+      include Messages
+
+      # @param [Hash] value
+      # @return [Result]
+      def self.validate(value)
+        value => { settings: Hash => settings }
+        settings => { vscode_extensions_gallery_metadata: Hash => extensions_gallery_metadata }
+
+        validatable_hash = make_hash_validatable_by_json_schemer(extensions_gallery_metadata)
+        errors = validate_against_schema(validatable_hash)
+
+        if errors.none?
+          Result.ok(value)
+        else
+          Result.err(SettingsVscodeExtensionsGalleryMetadataValidationFailed.new(details: errors.join(". ")))
+        end
+      end
+
+      # @param [Hash] hash
+      # @return [Hash]
+      def self.make_hash_validatable_by_json_schemer(hash)
+        hash
+          .deep_stringify_keys
+          .transform_values { |v| v.is_a?(Symbol) ? v.to_s : v }
+      end
+
+      # @param [Hash] hash_to_validate
+      # @return [Array]
+      def self.validate_against_schema(hash_to_validate)
+        schema = {
+          "properties" => {
+            "enabled" => {
+              "type" => "boolean"
+            }
+          },
+          # do conditional check that "enabled" is boolean type
+          "if" => {
+            "properties" => {
+              "enabled" => {
+                "type" => "boolean"
+              }
+            }
+          },
+          "then" => {
+            # "enabled" is boolean, do conditional check for "enabled" value
+            "if" => {
+              "properties" => {
+                "enabled" => {
+                  "const" => true
+                }
+              }
+            },
+            "then" => {
+              # "enabled" is true, "disabled_reason" is not required
+              "required" => %w[enabled]
+            },
+            "else" => {
+              # "enabled" is false, "disabled_reason" is required
+              "required" => %w[enabled disabled_reason],
+              "properties" => {
+                "disabled_reason" => {
+                  "type" => "string"
+                }
+              }
+            }
+          }
+        }
+
+        schemer = JSONSchemer.schema(schema)
+        errors = schemer.validate(hash_to_validate)
+        errors.map { |error| JSONSchemer::Errors.pretty(error) }
+      end
+    end
+  end
+end
diff --git a/ee/lib/remote_development/settings/extensions_gallery_validator.rb b/ee/lib/remote_development/settings/extensions_gallery_validator.rb
index aa44de52ec61ef239fb8b8e17cb9aae9ff4b0106..a3c158de793d6d7e20d27126ec44b9b5509b2d79 100644
--- a/ee/lib/remote_development/settings/extensions_gallery_validator.rb
+++ b/ee/lib/remote_development/settings/extensions_gallery_validator.rb
@@ -23,9 +23,9 @@ def self.validate(value)
         end
       end
 
-      # @param [Hash] json_to_validate
+      # @param [Hash] hash_to_validate
       # @return [Array]
-      def self.validate_against_schema(json_to_validate)
+      def self.validate_against_schema(hash_to_validate)
         schema = {
           "required" =>
             %w[
@@ -47,7 +47,7 @@ def self.validate_against_schema(json_to_validate)
         }
 
         schemer = JSONSchemer.schema(schema)
-        errors = schemer.validate(json_to_validate)
+        errors = schemer.validate(hash_to_validate)
         errors.map { |error| JSONSchemer::Errors.pretty(error) }
       end
     end
diff --git a/ee/lib/remote_development/settings/main.rb b/ee/lib/remote_development/settings/main.rb
index d0aa0734a5c65f5de6ed8ca733119e5c586646e0..b926f45196cb0cc6031d8746575e3fb7bb92c443 100644
--- a/ee/lib/remote_development/settings/main.rb
+++ b/ee/lib/remote_development/settings/main.rb
@@ -8,10 +8,11 @@ class Main
       extend MessageSupport
       private_class_method :generate_error_response_from_message
 
+      # @param [Hash] value
       # @return [Hash]
       # @raise [UnmatchedResultError]
-      def self.get_settings
-        initial_result = Result.ok({})
+      def self.get_settings(value)
+        initial_result = Result.ok(value)
 
         # The order of the chain determines the precedence of settings. I.e., defaults are
         # overridden by env vars, and any subsequent steps override env vars.
@@ -19,10 +20,12 @@ def self.get_settings
           initial_result
             .map(DefaultsInitializer.method(:init))
             .and_then(CurrentSettingsReader.method(:read))
+            .map(ExtensionsGalleryMetadataGenerator.method(:generate))
             # NOTE: EnvVarReader is kept as last step, so it can always be used to easily override any settings for
             #       local or temporary testing.
             .and_then(EnvVarReader.method(:read))
             .and_then(RemoteDevelopment::Settings::ExtensionsGalleryValidator.method(:validate))
+            .and_then(RemoteDevelopment::Settings::ExtensionsGalleryMetadataValidator.method(:validate))
             .map(
               # As the final step, return the settings in a SettingsGetSuccessful message
               ->(value) do
@@ -39,6 +42,8 @@ def self.get_settings
           generate_error_response_from_message(message: message, reason: :internal_server_error)
         in { err: SettingsVscodeExtensionsGalleryValidationFailed => message }
           generate_error_response_from_message(message: message, reason: :internal_server_error)
+        in { err: SettingsVscodeExtensionsGalleryMetadataValidationFailed => message }
+          generate_error_response_from_message(message: message, reason: :internal_server_error)
         in { ok: SettingsGetSuccessful => message }
           { settings: message.context.fetch(:settings), status: :success }
         else
diff --git a/ee/lib/remote_development/settings/public_api.rb b/ee/lib/remote_development/settings/public_api.rb
index 82febf6f576b282d8a443bb9d12bcff00faf7024..3152d5f68832acdaaaae473c591688f2c96a630a 100644
--- a/ee/lib/remote_development/settings/public_api.rb
+++ b/ee/lib/remote_development/settings/public_api.rb
@@ -11,21 +11,23 @@ module Settings
     # RemoteDevelopment::Settings::Main.get_settings
     module PublicApi
       # @param [Symbol] setting_name
+      # @param [Hash] options
       # @return [Object]
       # @raise [RuntimeError]
-      def get_single_setting(setting_name)
+      def get_single_setting(setting_name, options = {})
         raise "Setting name must be a Symbol" unless setting_name.is_a?(Symbol)
 
         is_valid_setting_name = get_all_settings.key?(setting_name)
         raise "Unsupported Remote Development setting name: '#{setting_name}'" unless is_valid_setting_name
 
-        get_all_settings.fetch(setting_name)
+        get_all_settings(options).fetch(setting_name)
       end
 
+      # @param [Hash] options
       # @return [Hash]
       # @raise [RuntimeError]
-      def get_all_settings
-        response_hash = RemoteDevelopment::Settings::Main.get_settings
+      def get_all_settings(options = {})
+        response_hash = RemoteDevelopment::Settings::Main.get_settings({ options: options })
 
         raise response_hash.fetch(:message).to_s if response_hash.fetch(:status) == :error
 
diff --git a/ee/spec/lib/remote_development/settings/extensions_gallery_metadata_generator_spec.rb b/ee/spec/lib/remote_development/settings/extensions_gallery_metadata_generator_spec.rb
new file mode 100644
index 0000000000000000000000000000000000000000..1969fbbe5a9912c5cb5a0b360b904c8b9669ecb1
--- /dev/null
+++ b/ee/spec/lib/remote_development/settings/extensions_gallery_metadata_generator_spec.rb
@@ -0,0 +1,81 @@
+# frozen_string_literal: true
+
+require 'spec_helper'
+
+RSpec.describe RemoteDevelopment::Settings::ExtensionsGalleryMetadataGenerator, :rd_fast, feature_category: :remote_development do
+  using RSpec::Parameterized::TableSyntax
+
+  let(:input_value) do
+    {
+      options: options,
+      settings: {
+        # NOTE: default value of 'vscode_extensions_gallery_metadata' is an empty hash. Include it here to
+        #       ensure that it always gets overwritten with the generated value
+        vscode_extensions_gallery_metadata: {},
+        some_other_existing_setting_that_should_not_be_overwritten: "some value"
+      }
+    }
+  end
+
+  subject(:returned_value) do
+    described_class.generate(input_value)
+  end
+
+  shared_examples 'extensions marketplace settings' do
+    it "has the expected settings behavior" do
+      if expected_vscode_extensions_gallery_metadata == RuntimeError
+        expected_err_msg = "Invalid user.extensions_marketplace_opt_in_status: '#{opt_in_status}'. " \
+          "Supported statuses are: [:unset, :enabled, :disabled]." # rubocop:disable Layout/LineEndStringConcatenationIndentation -- This is already changed in the next version of gitlab-styles
+        expect { returned_value }
+          .to raise_error(expected_err_msg)
+      else
+        expect(returned_value).to eq(
+          input_value.deep_merge(
+            settings: {
+              vscode_extensions_gallery_metadata: expected_vscode_extensions_gallery_metadata
+            }
+          )
+        )
+      end
+    end
+  end
+
+  where(
+    :user_exists,
+    :opt_in_status,
+    :flag_exists,
+    :flag_enabled,
+    :expected_vscode_extensions_gallery_metadata
+  ) do
+    # @formatter:off - Turn off RubyMine autoformatting
+
+    # user exists | opt_in_status | flag exists | flag_enabled | expected_settings
+    false         | :undefined    | false       | :undefined   | { enabled: false, disabled_reason: :no_user }
+    false         | :undefined    | true        | true         | { enabled: false, disabled_reason: :no_user }
+    true          | :unset        | false       | :undefined   | { enabled: false, disabled_reason: :no_flag }
+    true          | :unset        | true        | false        | { enabled: false, disabled_reason: :instance_disabled }
+    true          | :unset        | true        | true         | { enabled: false, disabled_reason: :opt_in_unset }
+    true          | :disabled     | true        | true         | { enabled: false, disabled_reason: :opt_in_disabled }
+    true          | :enabled      | true        | true         | { enabled: true }
+    true          | :invalid      | true        | true         | RuntimeError
+
+    # @formatter:on
+  end
+
+  with_them do
+    let(:user) { create(:user) }
+
+    let(:options) do
+      options = {}
+      options[:user] = user if user_exists
+      options[:vscode_extensions_marketplace_feature_flag_enabled] = flag_enabled if flag_exists
+      options
+    end
+
+    before do
+      allow(user).to receive(:extensions_marketplace_opt_in_status) { opt_in_status.to_s }
+    end
+
+    it_behaves_like "extensions marketplace settings"
+  end
+end
diff --git a/ee/spec/lib/remote_development/settings/extensions_gallery_metadata_validator_spec.rb b/ee/spec/lib/remote_development/settings/extensions_gallery_metadata_validator_spec.rb
new file mode 100644
index 0000000000000000000000000000000000000000..e3fb3bdb5c6cb040cce3a063f4f2019fef2ee25f
--- /dev/null
+++ b/ee/spec/lib/remote_development/settings/extensions_gallery_metadata_validator_spec.rb
@@ -0,0 +1,109 @@
+# frozen_string_literal: true
+
+require_relative "../rd_fast_spec_helper"
+
+RSpec.describe RemoteDevelopment::Settings::ExtensionsGalleryMetadataValidator, :rd_fast, feature_category: :remote_development do
+  include ResultMatchers
+
+  let(:value) do
+    {
+      settings: {
+        vscode_extensions_gallery_metadata: extensions_gallery_metadata
+      }
+    }
+  end
+
+  subject(:result) do
+    described_class.validate(value)
+  end
+
+  context "when vscode_extensions_gallery_metadata is valid" do
+    shared_examples "success result" do
+      it "return an ok Result containing the original value which was passed" do
+        expect(result).to eq(Result.ok(value))
+      end
+    end
+
+    context "when enabled is true" do
+      let(:extensions_gallery_metadata) do
+        {
+          enabled: true
+        }
+      end
+
+      it_behaves_like 'success result'
+    end
+
+    context "when enabled is false and disabled_reason is present" do
+      let(:extensions_gallery_metadata) do
+        {
+          enabled: false,
+          disabled_reason: :no_user
+        }
+      end
+
+      it_behaves_like 'success result'
+    end
+  end
+
+  context "when vscode_extensions_gallery_metadata is invalid" do
+    shared_examples "err result" do |expected_error_details:|
+      it "returns an err Result containing error details" do
+        expect(result).to be_err_result do |message|
+          expect(message)
+            .to be_a(RemoteDevelopment::Messages::SettingsVscodeExtensionsGalleryMetadataValidationFailed)
+          message.context => { details: String => error_details }
+          expect(error_details).to eq(expected_error_details)
+        end
+      end
+    end
+
+    context "when empty" do
+      let(:extensions_gallery_metadata) { {} }
+
+      it_behaves_like "err result", expected_error_details: "root is missing required keys: enabled"
+    end
+
+    context "when enabled is missing but disabled_reason is present" do
+      let(:extensions_gallery_metadata) { { disabled_reason: :no_user } }
+
+      it_behaves_like "err result", expected_error_details: "root is missing required keys: enabled"
+    end
+
+    context "when enabled is false but disabled_reason is missing" do
+      let(:extensions_gallery_metadata) do
+        {
+          enabled: false
+        }
+      end
+
+      it_behaves_like "err result", expected_error_details: "root is missing required keys: disabled_reason"
+    end
+
+    context "for enabled" do
+      context "when not a boolean" do
+        let(:extensions_gallery_metadata) do
+          {
+            enabled: "not a boolean"
+          }
+        end
+
+        it_behaves_like "err result", expected_error_details: "property '/enabled' is not of type: boolean"
+      end
+    end
+
+    context "for disabled_reason" do
+      context "when not a string" do
+        let(:extensions_gallery_metadata) do
+          {
+            enabled: false,
+            disabled_reason: 1
+          }
+        end
+
+        it_behaves_like "err result", expected_error_details:
+          "property '/disabled_reason' is not of type: string"
+      end
+    end
+  end
+end
diff --git a/ee/spec/lib/remote_development/settings/extensions_gallery_validator_spec.rb b/ee/spec/lib/remote_development/settings/extensions_gallery_validator_spec.rb
index 25eea0572e2b48e68b03c5daba3e5dbfa53c53fa..22156d6c05e24c555c8dc4cc8026b6181e0d4bbf 100644
--- a/ee/spec/lib/remote_development/settings/extensions_gallery_validator_spec.rb
+++ b/ee/spec/lib/remote_development/settings/extensions_gallery_validator_spec.rb
@@ -55,16 +55,14 @@
       let(:vscode_extensions_gallery) { {} }
 
       it_behaves_like "err result", expected_error_details:
-        "root is missing required keys: service_url, item_url, " \
-          "resource_url_template" # rubocop:disable Layout/LineEndStringConcatenationIndentation -- This is being changed in https://gitlab.com/gitlab-org/ruby/gems/gitlab-styles/-/merge_requests/212
+        "root is missing required keys: service_url, item_url, resource_url_template"
     end
 
     context "for service_url" do
       context "when not a string" do
         let(:service_url) { { not_a_string: true } }
 
-        it_behaves_like "err result", expected_error_details:
-          "property '/service_url' is not of type: string"
+        it_behaves_like "err result", expected_error_details: "property '/service_url' is not of type: string"
       end
     end
 
@@ -72,8 +70,7 @@
       context "when not a string" do
         let(:item_url) { { not_a_string: true } }
 
-        it_behaves_like "err result", expected_error_details:
-          "property '/item_url' is not of type: string"
+        it_behaves_like "err result", expected_error_details: "property '/item_url' is not of type: string"
       end
     end
 
@@ -81,8 +78,7 @@
       context "when not a string" do
         let(:resource_url_template) { { not_a_string: true } }
 
-        it_behaves_like "err result", expected_error_details:
-          "property '/resource_url_template' is not of type: string"
+        it_behaves_like "err result", expected_error_details: "property '/resource_url_template' is not of type: string"
       end
     end
   end
diff --git a/ee/spec/lib/remote_development/settings/main_spec.rb b/ee/spec/lib/remote_development/settings/main_spec.rb
index b38c56466724c98156c8acd6d62b0e64fe0c0e43..7b47c58573a0e10fc2c0591639c0c50a82e7ea78 100644
--- a/ee/spec/lib/remote_development/settings/main_spec.rb
+++ b/ee/spec/lib/remote_development/settings/main_spec.rb
@@ -5,46 +5,56 @@
 RSpec.describe RemoteDevelopment::Settings::Main, :rd_fast, feature_category: :remote_development do
   include RemoteDevelopment::RailwayOrientedProgrammingHelpers
 
+  let(:input_value) { { some_context: true } }
   let(:settings) { { some_setting: 42 } }
-  let(:value) { { settings: settings } }
+  let(:value) { { some_context: true, settings: settings } }
   let(:error_details) { 'some error details' }
   let(:err_message_context) { { details: error_details } }
 
+  # rubocop:disable Layout/LineLength -- keep all the class and method fixtures as single-liners easier scanning/editing
   # Classes
 
   let(:defaults_initializer_class) { RemoteDevelopment::Settings::DefaultsInitializer }
   let(:current_settings_reader_class) { RemoteDevelopment::Settings::CurrentSettingsReader }
+  let(:extensions_gallery_metadata_generator_class) { RemoteDevelopment::Settings::ExtensionsGalleryMetadataGenerator }
   let(:env_var_reader_class) { RemoteDevelopment::Settings::EnvVarReader }
   let(:extensions_gallery_validator_class) { RemoteDevelopment::Settings::ExtensionsGalleryValidator }
+  let(:extensions_gallery_metadata_validator_class) { RemoteDevelopment::Settings::ExtensionsGalleryMetadataValidator }
 
   # Methods
 
   let(:defaults_initializer_method) { defaults_initializer_class.singleton_method(:init) }
   let(:current_settings_reader_method) { current_settings_reader_class.singleton_method(:read) }
+  let(:extensions_gallery_metadata_generator_method) { extensions_gallery_metadata_generator_class.singleton_method(:generate) }
   let(:env_var_reader_method) { env_var_reader_class.singleton_method(:read) }
-  let(:extensions_gallery_validator_method) do
-    extensions_gallery_validator_class.singleton_method(:validate)
-  end
+  let(:extensions_gallery_validator_method) { extensions_gallery_validator_class.singleton_method(:validate) }
+  let(:extensions_gallery_metadata_validator_method) { extensions_gallery_metadata_validator_class.singleton_method(:validate) }
 
   # Subject
 
-  subject(:response) { described_class.get_settings }
+  subject(:response) { described_class.get_settings(input_value) }
 
   before do
     allow(defaults_initializer_class).to receive(:method).with(:init) { defaults_initializer_method }
     allow(current_settings_reader_class).to receive(:method).with(:read) { current_settings_reader_method }
+    allow(extensions_gallery_metadata_generator_class).to(receive(:method).with(:generate)) { extensions_gallery_metadata_generator_method }
     allow(env_var_reader_class).to receive(:method).with(:read) { env_var_reader_method }
-    allow(extensions_gallery_validator_class).to receive(:method).with(:validate) do
-      extensions_gallery_validator_method
-    end
+    allow(extensions_gallery_validator_class).to(receive(:method).with(:validate)) { extensions_gallery_validator_method }
+    allow(extensions_gallery_metadata_validator_class).to(receive(:method).with(:validate)) { extensions_gallery_metadata_validator_method }
 
-    stub_method_to_modify_and_return_value(defaults_initializer_method, expected_value: {}, returned_value: value)
+    stub_method_to_modify_and_return_value(defaults_initializer_method, expected_value: input_value, returned_value: value)
+    stub_methods_to_return_value(extensions_gallery_metadata_generator_method)
   end
+  # rubocop:enable Layout/LineLength
 
   context 'when all steps are successful' do
     before do
-      stub_methods_to_return_ok_result(current_settings_reader_method, env_var_reader_method,
-        extensions_gallery_validator_method)
+      stub_methods_to_return_ok_result(
+        current_settings_reader_method,
+        env_var_reader_method,
+        extensions_gallery_validator_method,
+        extensions_gallery_metadata_validator_method
+      )
     end
 
     it 'returns a success response with the settings as the payload' do
@@ -108,6 +118,28 @@
     end
   end
 
+  context 'when the ExtensionsGalleryMetadataValidator returns an err Result' do
+    before do
+      stub_methods_to_return_ok_result(
+        current_settings_reader_method,
+        env_var_reader_method,
+        extensions_gallery_validator_method
+      )
+      stub_methods_to_return_err_result(
+        method: extensions_gallery_metadata_validator_method,
+        message_class: RemoteDevelopment::Messages::SettingsVscodeExtensionsGalleryMetadataValidationFailed
+      )
+    end
+
+    it 'returns an error response' do
+      expect(response).to eq({
+        status: :error,
+        message: "Settings VSCode extensions gallery metadata validation failed: #{error_details}",
+        reason: :internal_server_error
+      })
+    end
+  end
+
   context 'when an invalid Result is returned' do
     before do
       stub_methods_to_return_ok_result(current_settings_reader_method)
diff --git a/ee/spec/lib/remote_development/settings/public_api_spec.rb b/ee/spec/lib/remote_development/settings/public_api_spec.rb
index da0bd5536c60c1ff538e13f9965a4f835e53fe29..344bb24e2988ba6c183ec132cd89439fa3121952 100644
--- a/ee/spec/lib/remote_development/settings/public_api_spec.rb
+++ b/ee/spec/lib/remote_development/settings/public_api_spec.rb
@@ -1,27 +1,52 @@
 # frozen_string_literal: true
 
-require 'spec_helper'
+require_relative '../rd_fast_spec_helper'
 
-RSpec.describe RemoteDevelopment::Settings::PublicApi, feature_category: :remote_development do
-  describe "get_single_setting" do
-    context "when passed a valid setting name" do
-      it "returns the setting value" do
-        expect(RemoteDevelopment::Settings.get_single_setting(:max_hours_before_termination_limit)).to eq(120)
+RSpec.describe RemoteDevelopment::Settings::PublicApi, :rd_fast, feature_category: :remote_development do
+  subject(:settings_module) { RemoteDevelopment::Settings }
+
+  before do
+    allow(RemoteDevelopment::Settings::Main).to receive(:get_settings).with({ options: {} }).and_return(response_hash)
+  end
+
+  context "when successful" do
+    let(:response_hash) { { settings: { some_setting: 42 }, status: :success } }
+
+    describe "get_single_setting" do
+      context "when passed a valid setting name" do
+        it "returns the setting value" do
+          expect(settings_module.get_single_setting(:some_setting)).to eq(42)
+        end
+      end
+
+      context "when passed options" do
+        let(:options) { { some_options_key: true } }
+
+        it "passes along the options and returns the setting value" do
+          expect(settings_module::Main).to receive(:get_settings).with({ options: options }).and_return(response_hash)
+          expect(settings_module.get_single_setting(:some_setting, options)).to eq(42)
+        end
       end
     end
 
-    context "when passed an invalid setting name" do
-      it "raises an exception with a descriptive message" do
-        expect { RemoteDevelopment::Settings.get_single_setting(:invalid_setting_name) }
-          .to raise_error("Unsupported Remote Development setting name: 'invalid_setting_name'")
+    describe "get_all_settings" do
+      it "returns a Hash containing all settings" do
+        expect(settings_module.get_all_settings)
+          .to match(hash_including(some_setting: 42))
       end
     end
   end
 
-  describe "get_all_settings" do
-    it "returns a Hash containing all settings" do
-      expect(RemoteDevelopment::Settings.get_all_settings)
-        .to match(hash_including(max_hours_before_termination_limit: 120))
+  context "when unsuccessful" do
+    let(:response_hash) { { status: :error, message: :failed } }
+
+    describe "get_single_setting" do
+      context "when passed an invalid setting name" do
+        it "raises an exception with a descriptive message" do
+          expect { settings_module.get_single_setting(:invalid_setting_name) }
+            .to raise_error("failed")
+        end
+      end
     end
   end
 end
diff --git a/ee/spec/lib/remote_development/settings/settings_integration_spec.rb b/ee/spec/lib/remote_development/settings/settings_integration_spec.rb
index 380d8545a460aa34e1527eb93e0dac6d9143bbd7..08b0c182896b7fe8ec645897f676a7b35a0cec00 100644
--- a/ee/spec/lib/remote_development/settings/settings_integration_spec.rb
+++ b/ee/spec/lib/remote_development/settings/settings_integration_spec.rb
@@ -3,9 +3,7 @@
 require 'spec_helper'
 
 RSpec.describe ::RemoteDevelopment::Settings, feature_category: :remote_development do # rubocop:disable RSpec/FilePath -- Not sure why this is being flagged
-  subject(:settings_module) do
-    described_class
-  end
+  subject(:settings_module) { described_class }
 
   context "when there is no override" do
     before do
@@ -47,4 +45,74 @@
       expect(settings_module.get_single_setting(:default_branch_name)).to eq(override_value_from_env)
     end
   end
+
+  context "when passed an invalid setting name" do
+    it "uses default value" do
+      expect { settings_module.get_single_setting(:invalid_setting_name) }
+        .to raise_error("Unsupported Remote Development setting name: 'invalid_setting_name'")
+    end
+  end
+
+  context "for vscode_extensions_gallery setting" do
+    subject(:vscode_extensions_gallery_setting) { settings_module.get_single_setting(:vscode_extensions_gallery) }
+
+    it "uses default value" do
+      expected_value = {
+        item_url: "https://open-vsx.org/vscode/item",
+        resource_url_template: "https://open-vsx.org/api/{publisher}/{name}/{version}/file/{path}",
+        service_url: "https://open-vsx.org/vscode/gallery"
+      }
+
+      expect(vscode_extensions_gallery_setting).to eq(expected_value)
+    end
+
+    context "when invalid value is set" do
+      before do
+        stub_env("GITLAB_REMOTE_DEVELOPMENT_VSCODE_EXTENSIONS_GALLERY", '{"foo":"bar"}')
+      end
+
+      it "raises an error" do
+        expected_err_msg = "Settings VSCode extensions gallery validation failed: root is missing required keys: " \
+          "service_url, item_url, resource_url_template" # rubocop:disable Layout/LineEndStringConcatenationIndentation -- This is being changed in https://gitlab.com/gitlab-org/ruby/gems/gitlab-styles/-/merge_requests/212
+        expect { vscode_extensions_gallery_setting }
+          .to raise_error(expected_err_msg)
+      end
+    end
+  end
+
+  context "for vscode_extensions_gallery_metadata setting" do
+    let_it_be(:user) { create(:user) }
+    let_it_be(:options) do
+      {
+        user: user,
+        vscode_extensions_marketplace_feature_flag_enabled: false
+      }
+    end
+
+    subject(:vscode_extensions_gallery_metadata_setting) do
+      settings_module.get_single_setting(:vscode_extensions_gallery_metadata, options)
+    end
+
+    it "uses default value" do
+      expected_value = {
+        enabled: false,
+        disabled_reason: :instance_disabled
+      }
+
+      expect(vscode_extensions_gallery_metadata_setting).to eq(expected_value)
+    end
+
+    context "when invalid value is set" do
+      before do
+        stub_env("GITLAB_REMOTE_DEVELOPMENT_VSCODE_EXTENSIONS_GALLERY_METADATA", '{"foo":"bar"}')
+      end
+
+      it "raises an error" do
+        expected_err_msg = "Settings VSCode extensions gallery metadata validation failed: " \
+          "root is missing required keys: enabled" # rubocop:disable Layout/LineEndStringConcatenationIndentation -- This is being changed in https://gitlab.com/gitlab-org/ruby/gems/gitlab-styles/-/merge_requests/212
+        expect { vscode_extensions_gallery_metadata_setting }
+          .to raise_error(expected_err_msg)
+      end
+    end
+  end
 end