diff --git a/lib/rubygems/resolver/api_specification.rb b/lib/rubygems/resolver/api_specification.rb
index a14bcbfeb1a6..8772c103beee 100644
--- a/lib/rubygems/resolver/api_specification.rb
+++ b/lib/rubygems/resolver/api_specification.rb
@@ -87,19 +87,24 @@ def pretty_print(q) # :nodoc:
   # Fetches a Gem::Specification for this APISpecification.
 
   def spec # :nodoc:
-    @spec ||=
-      begin
-        tuple = Gem::NameTuple.new @name, @version, @platform
-        source.fetch_spec tuple
-      rescue Gem::RemoteFetcher::FetchError
-        raise if @original_platform == @platform
-
-        tuple = Gem::NameTuple.new @name, @version, @original_platform
-        source.fetch_spec tuple
-      end
+    @spec ||= build_minimal_spec_from_compact_index
   end
 
   def source # :nodoc:
     @set.source
   end
+
+  private
+
+  def build_minimal_spec_from_compact_index
+    spec = Gem::Specification.new
+    spec.name = @name
+    spec.version = @version
+    spec.platform = @platform
+    spec.dependencies.replace(@dependencies)
+    spec.required_ruby_version = @required_ruby_version
+    spec.required_rubygems_version = @required_rubygems_version
+
+    spec
+  end
 end
diff --git a/test/rubygems/helper.rb b/test/rubygems/helper.rb
index dc40f4ecb1f8..4d2f889d1b46 100644
--- a/test/rubygems/helper.rb
+++ b/test/rubygems/helper.rb
@@ -1143,6 +1143,25 @@ def write_marshalled_gemspecs(*all_specs)
     end
   end
 
+  ##
+  # Sets up Compact Index API endpoints for testing. Does NOT set up old marshal API.
+  # This causes Source#new_dependency_resolver_set to use APISet.
+  #
+  # Usage:
+  #   compact_index do |ci|
+  #     ci.gem "a", 1 do |s|
+  #       s.add_dependency "b", ">= 2.0"
+  #     end
+  #     ci.gem "b", 2
+  #   end
+
+  def compact_index(&block)
+    fake_compact_index = Gem::TestCase::CompactIndexSetup.new(self, @gem_repo)
+    yield fake_compact_index
+    fake_compact_index.stub
+    fake_compact_index.specs
+  end
+
   ##
   # Deflates +data+
 
diff --git a/test/rubygems/test_gem_commands_install_command.rb b/test/rubygems/test_gem_commands_install_command.rb
index d2ca933a632c..617c678f6c00 100644
--- a/test/rubygems/test_gem_commands_install_command.rb
+++ b/test/rubygems/test_gem_commands_install_command.rb
@@ -29,9 +29,9 @@ def teardown
   end
 
   def test_execute_exclude_prerelease
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", 2
-      fetcher.gem "a", "2.pre"
+    compact_index do |ci|
+      ci.gem "a", 2
+      ci.gem "a", "2.pre"
     end
 
     @cmd.options[:args] = %w[a]
@@ -46,9 +46,9 @@ def test_execute_exclude_prerelease
   end
 
   def test_execute_explicit_version_includes_prerelease
-    specs = spec_fetcher do |fetcher|
-      fetcher.gem "a", 2
-      fetcher.gem "a", "2.a"
+    specs = compact_index do |ci|
+      ci.gem "a", 2
+      ci.gem "a", "2.a"
     end
 
     a2_pre = specs["a-2.a"]
@@ -430,9 +430,9 @@ def test_execute_nonexistent_with_dashes
   end
 
   def test_execute_prerelease_skipped_when_no_flag_set
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", 1
-      fetcher.gem "a", "3.a"
+    compact_index do |ci|
+      ci.gem "a", 1
+      ci.gem "a", "3.a"
     end
 
     @cmd.options[:prerelease] = false
@@ -483,9 +483,9 @@ def test_execute_with_version_specified_by_colon
   end
 
   def test_execute_prerelease_skipped_when_non_pre_available
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", "2.pre"
-      fetcher.gem "a", 2
+    compact_index do |ci|
+      ci.gem "a", "2.pre"
+      ci.gem "a", 2
     end
 
     @cmd.options[:prerelease] = true
@@ -532,9 +532,9 @@ def test_execute_required_ruby_version
 
   def test_execute_required_ruby_version_upper_bound
     local = Gem::Platform.local
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", 2.0
-      fetcher.gem "a", 2.0 do |s|
+    compact_index do |ci|
+      ci.gem "a", 2.0
+      ci.gem "a", 2.0 do |s|
         s.required_ruby_version = "< #{RUBY_VERSION}.a"
         s.platform = local
       end
@@ -552,8 +552,8 @@ def test_execute_required_ruby_version_upper_bound
   end
 
   def test_execute_required_ruby_version_specific_not_met
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", "1.0" do |s|
+    compact_index do |ci|
+      ci.gem "a", "1.0" do |s|
         s.required_ruby_version = "= 1.4.6"
       end
     end
@@ -572,8 +572,8 @@ def test_execute_required_ruby_version_specific_not_met
   end
 
   def test_execute_required_ruby_version_specific_prerelease_met
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", "1.0" do |s|
+    compact_index do |ci|
+      ci.gem "a", "1.0" do |s|
         s.required_ruby_version = ">= 1.4.6.preview2"
       end
     end
@@ -592,8 +592,8 @@ def test_execute_required_ruby_version_specific_prerelease_met
   def test_execute_required_ruby_version_specific_prerelease_not_met
     next_ruby_pre = Gem.ruby_version.segments.map.with_index {|n, i| i == 1 ? n + 1 : n }.join(".") + ".a"
 
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", "1.0" do |s|
+    compact_index do |ci|
+      ci.gem "a", "1.0" do |s|
         s.required_ruby_version = "> #{next_ruby_pre}"
       end
     end
@@ -612,8 +612,8 @@ def test_execute_required_ruby_version_specific_prerelease_not_met
   end
 
   def test_execute_required_rubygems_version_wrong
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", "1.0" do |s|
+    compact_index do |ci|
+      ci.gem "a", "1.0" do |s|
         s.required_rubygems_version = "< 0"
       end
     end
@@ -632,8 +632,8 @@ def test_execute_required_rubygems_version_wrong
   end
 
   def test_execute_rdoc
-    specs = spec_fetcher do |fetcher|
-      fetcher.gem "a", 2
+    specs = compact_index do |ci|
+      ci.gem "a", 2
     end
 
     Gem.done_installing(&Gem::RDoc.method(:generation_hook))
@@ -661,8 +661,8 @@ def test_execute_rdoc
   end if defined?(Gem::RDoc) && !Gem.rdoc_hooks_defined_via_plugin?
 
   def test_execute_rdoc_with_path
-    specs = spec_fetcher do |fetcher|
-      fetcher.gem "a", 2
+    specs = compact_index do |ci|
+      ci.gem "a", 2
     end
 
     Gem.done_installing(&Gem::RDoc.method(:generation_hook))
@@ -690,8 +690,8 @@ def test_execute_rdoc_with_path
   end if defined?(Gem::RDoc) && !Gem.rdoc_hooks_defined_via_plugin?
 
   def test_execute_saves_build_args
-    specs = spec_fetcher do |fetcher|
-      fetcher.gem "a", 2
+    specs = compact_index do |ci|
+      ci.gem "a", 2
     end
 
     args = %w[--with-awesome=true --more-awesome=yes]
@@ -720,8 +720,8 @@ def test_execute_saves_build_args
   end
 
   def test_execute_remote
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", 2
+    compact_index do |ci|
+      ci.gem "a", 2
     end
 
     @cmd.options[:args] = %w[a]
@@ -740,8 +740,8 @@ def test_execute_remote
   def test_execute_with_invalid_gem_file
     FileUtils.touch("a.gem")
 
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", 2
+    compact_index do |ci|
+      ci.gem "a", 2
     end
 
     @cmd.options[:args] = %w[a]
@@ -758,8 +758,8 @@ def test_execute_with_invalid_gem_file
   end
 
   def test_execute_remote_truncates_existing_gemspecs
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", 1
+    compact_index do |ci|
+      ci.gem "a", 1
     end
 
     @cmd.options[:domain] = :remote
@@ -791,9 +791,9 @@ def test_execute_remote_truncates_existing_gemspecs
   end
 
   def test_execute_remote_ignores_files
-    specs = spec_fetcher do |fetcher|
-      fetcher.gem "a", 1
-      fetcher.gem "a", 2
+    specs = compact_index do |ci|
+      ci.gem "a", 1
+      ci.gem "a", 2
     end
 
     @cmd.options[:domain] = :remote
@@ -887,11 +887,11 @@ def test_execute_two_version
   end
 
   def test_execute_two_version_specified_by_colon
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", 1
-      fetcher.gem "a", 2
-      fetcher.gem "b", 1
-      fetcher.gem "b", 2
+    compact_index do |ci|
+      ci.gem "a", 1
+      ci.gem "a", 2
+      ci.gem "b", 1
+      ci.gem "b", 2
     end
 
     @cmd.options[:args] = %w[a:1 b:1]
@@ -956,8 +956,8 @@ def test_install_gem_ignore_dependencies_both
   end
 
   def test_install_gem_ignore_dependencies_remote
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", 2
+    compact_index do |ci|
+      ci.gem "a", 2
     end
 
     @cmd.options[:ignore_dependencies] = true
@@ -969,10 +969,10 @@ def test_install_gem_ignore_dependencies_remote
 
   def test_install_gem_ignore_dependencies_remote_platform_local
     local = Gem::Platform.local
-    spec_fetcher do |fetcher|
-      fetcher.gem "a", 3
+    compact_index do |ci|
+      ci.gem "a", 3
 
-      fetcher.gem "a", 3 do |s|
+      ci.gem "a", 3 do |s|
         s.platform = local
       end
     end
@@ -1365,9 +1365,9 @@ def test_execute_with_gemdeps_path_ignores_system
   end
 
   def test_execute_uses_deps_a_gemdeps_with_a_path
-    specs = spec_fetcher do |fetcher|
-      fetcher.gem "q", "1.0"
-      fetcher.gem "r", "2.0", "q" => nil
+    specs = compact_index do |ci|
+      ci.gem "q", "1.0"
+      ci.gem "r", "2.0", "q" => nil
     end
 
     i = Gem::Installer.at specs["q-1.0"].cache_file, install_dir: "gf-path"
@@ -1568,8 +1568,8 @@ def test_explain_platform_ruby_ignore_dependencies
 
   def test_suggest_update_if_enabled
     TestUpdateSuggestion.with_eligible_environment(cmd: @cmd) do
-      spec_fetcher do |fetcher|
-        fetcher.gem "a", 2
+      compact_index do |ci|
+        ci.gem "a", 2
       end
 
       @cmd.options[:args] = %w[a]
@@ -1642,4 +1642,32 @@ def test_execute_bindir_with_nonexistent_parent_dirs
 
     assert_equal %w[a-2], @cmd.installed_specs.map(&:full_name)
   end
+
+  def test_install_from_compact_index_only_source
+    compact_index do |ci|
+      ci.gem "main-gem", "2" do |s|
+        s.add_dependency "dep-gem", ">= 1.0"
+      end
+      ci.gem "dep-gem", "1"
+    end
+
+    @cmd.options[:args] = %w[main-gem]
+
+    use_ui @ui do
+      assert_raise Gem::MockGemUi::SystemExitException, @ui.error do
+        @cmd.execute
+      end
+    end
+
+    assert_equal %w[dep-gem-1 main-gem-2], @cmd.installed_specs.map(&:full_name).sort
+
+    installed_gem = @cmd.installed_specs.find {|s| s.name == "main-gem" }
+    assert_equal "main-gem", installed_gem.name
+    assert_equal Gem::Version.new("2"), installed_gem.version
+    assert_equal 1, installed_gem.dependencies.size
+    assert_equal "dep-gem", installed_gem.dependencies.first.name
+
+    marshal_requests = @fetcher.paths.select {|p| p.include?("/quick/Marshal.4.8/") }
+    assert_empty marshal_requests, "Should not request marshal gemspecs: #{marshal_requests.inspect}"
+  end
 end
diff --git a/test/rubygems/test_gem_resolver_api_specification.rb b/test/rubygems/test_gem_resolver_api_specification.rb
index 2119d734780b..766623049783 100644
--- a/test/rubygems/test_gem_resolver_api_specification.rb
+++ b/test/rubygems/test_gem_resolver_api_specification.rb
@@ -164,4 +164,55 @@ def test_spec_jruby_platform
     assert_kind_of Gem::Specification, spec
     assert_equal "j-1-java", spec.full_name
   end
+
+  def test_spec_builds_from_compact_index_without_marshal_gemspec
+    dep_uri = @gem_repo + "info"
+    set = Gem::Resolver::APISet.new dep_uri
+    data = {
+      name: "rails",
+      number: "7.0.0",
+      platform: "ruby",
+      dependencies: [
+        ["activesupport", "= 7.0.0"],
+        ["bundler", ">= 1.15.0"],
+      ],
+      requirements: {
+        ruby: ">= 3.4.0",
+        rubygems: ">= 4.0.0",
+      },
+    }
+
+    api_spec = Gem::Resolver::APISpecification.new set, data
+    spec = api_spec.spec
+
+    assert_kind_of Gem::Specification, spec
+    assert_equal "rails", spec.name
+    assert_equal Gem::Version.new("7.0.0"), spec.version
+    assert_equal Gem::Platform::RUBY, spec.platform
+
+    assert_equal 2, spec.dependencies.size
+    assert spec.dependencies.any? {|d| d.name == "activesupport" && d.requirement.to_s == "= 7.0.0" }
+    assert spec.dependencies.any? {|d| d.name == "bundler" && d.requirement.to_s == ">= 1.15.0" }
+
+    assert_equal ">= 3.4.0", spec.required_ruby_version.to_s
+    assert_equal ">= 4.0.0", spec.required_rubygems_version.to_s
+  end
+
+  def test_spec_builds_without_requirements
+    dep_uri = @gem_repo + "info"
+    set = Gem::Resolver::APISet.new dep_uri
+    data = {
+      name: "simple_gem",
+      number: "1.0.0",
+      platform: "ruby",
+      dependencies: [],
+    }
+
+    api_spec = Gem::Resolver::APISpecification.new set, data
+    spec = api_spec.spec
+
+    assert_kind_of Gem::Specification, spec
+    assert_equal "simple_gem", spec.name
+    assert_equal Gem::Version.new("1.0.0"), spec.version
+  end
 end
diff --git a/test/rubygems/utilities.rb b/test/rubygems/utilities.rb
index bf601f6fac2d..124dbc9579c1 100644
--- a/test/rubygems/utilities.rb
+++ b/test/rubygems/utilities.rb
@@ -420,6 +420,106 @@ def write_spec(spec) # :nodoc:
   end
 end
 
+##
+# Minimal CompactIndex implementation for tests.
+# This is a simplified version that only implements what's needed for test fixtures.
+module CompactIndexBuilder
+  # Generates the /info/{gem_name} response body
+  # Format: ---\nVERSION DEPS|METADATA\n
+  # Where DEPS is: dep_name:requirement,dep_name:requirement
+  # And METADATA is: checksum:SHA256,ruby:requirement,rubygems:requirement
+  def self.info(versions)
+    lines = ["---"]
+    versions.each do |version|
+      # Add dependencies (if any)
+      deps = version.dependencies.map {|d| "#{d.name}:#{d.requirement}" }
+      deps_string = deps.join(",")
+
+      # Build metadata
+      metadata = []
+      metadata << "checksum:#{version.checksum}" if version.checksum
+      metadata << "ruby:#{version.ruby_version}" if version.ruby_version && version.ruby_version != ">= 0"
+      metadata << "rubygems:#{version.rubygems_version}" if version.rubygems_version && version.rubygems_version != ">= 0"
+
+      # Format: "VERSION DEPS|METADATA" or "VERSION |METADATA" (space before | only when no deps)
+      line = "#{version.version} #{deps_string}|" + metadata.join(",")
+      lines << line
+    end
+    lines.join("\n") << "\n"
+  end
+
+  GemVersion = Data.define(:version, :platform, :checksum, :info_checksum, :dependencies, :ruby_version, :rubygems_version) do
+    def initialize(version:, platform:, checksum:, info_checksum: nil, dependencies: [], ruby_version: nil, rubygems_version: nil)
+      super(version:, platform:, checksum:, info_checksum:, dependencies:, ruby_version:, rubygems_version:)
+    end
+  end
+
+  Dependency = Data.define(:name, :requirement)
+end
+
+##
+# The CompactIndexSetup allows easy setup of compact index endpoints in tests.
+# Unlike SpecFetcherSetup, this only sets up compact index (no marshal API).
+#
+#   compact_index do |ci|
+#     ci.gem "a", 1 do |s|
+#       s.add_dependency "b", "~> 2.0"
+#     end
+#     ci.gem "b", 2
+#   end
+
+class Gem::TestCase::CompactIndexSetup
+  attr_reader :specs
+
+  def initialize(test, repository)
+    @test = test
+    @repository = repository
+    @test.fetcher = Gem::FakeFetcher.new
+    Gem::RemoteFetcher.fetcher = @test.fetcher
+    @specs = {}
+  end
+
+  def gem(name, version, dependencies = nil, &block)
+    spec = @test.util_spec(name, version, dependencies, &block)
+    @specs[spec.full_name] = spec
+  end
+
+  def stub
+    @specs.values.group_by(&:name).each do |name, gem_specs|
+      versions = gem_specs.map do |spec|
+        gem_file = Gem::Package.build(spec)
+        gem_contents = Gem.read_binary(gem_file)
+        FileUtils.cp gem_file, spec.cache_file
+
+        @test.fetcher.data["#{@repository}gems/#{spec.file_name}"] = gem_contents
+
+        dependencies = spec.dependencies.select(&:runtime?).map do |dep|
+          CompactIndexBuilder::Dependency.new(dep.name, dep.requirement.to_s)
+        end
+
+        checksum = Digest::SHA256.hexdigest(gem_contents)
+
+        CompactIndexBuilder::GemVersion.new(
+          spec.version.to_s,
+          spec.platform.to_s,
+          checksum,
+          nil,
+          dependencies,
+          spec.required_ruby_version.to_s,
+          spec.required_rubygems_version.to_s
+        )
+      end
+
+      @test.fetcher.data["#{@repository}info/#{name}"] = CompactIndexBuilder.info(versions)
+    end
+
+    # stub only to pass Compact Index API presence check currently
+    versions_response = Gem::Net::HTTPResponse.new "1.1", 200, "OK"
+    versions_response.uri = Gem::URI("#{@repository}versions")
+    @test.fetcher.data["#{@repository}versions"] = versions_response
+  end
+end
+
 ##
 # A StringIO duck-typed class that uses Tempfile instead of String as the
 # backing store.