diff --git a/Library/Homebrew/api.rb b/Library/Homebrew/api.rb
index e4028b26781eb..a6dadf6fa6c3f 100644
--- a/Library/Homebrew/api.rb
+++ b/Library/Homebrew/api.rb
@@ -21,6 +21,7 @@ module API
 
     API_DOMAIN = "https://formulae.brew.sh/api"
     HOMEBREW_CACHE_API = (HOMEBREW_CACHE/"api").freeze
+    MAX_RETRIES = 3
 
     sig { params(endpoint: String, json: T::Boolean).returns(T.any(String, Hash)) }
     def fetch(endpoint, json: true)
@@ -38,5 +39,24 @@ def fetch(endpoint, json: true)
     rescue JSON::ParserError
       raise ArgumentError, "Invalid JSON file: #{Tty.underline}#{api_url}#{Tty.reset}"
     end
+
+    def fetch_json_api_file(endpoint, target:)
+      retry_count = 0
+
+      url = "#{API_DOMAIN}/#{endpoint}"
+      begin
+        curl_args = %W[--compressed --silent #{url}]
+        curl_args.prepend("--time-cond", target) if target.exist? && !target.empty?
+        Utils::Curl.curl_download(*curl_args, to: target, max_time: 5)
+
+        JSON.parse(target.read)
+      rescue JSON::ParserError
+        target.unlink
+        retry_count += 1
+        odie "Cannot download non-corrupt #{url}!" if retry_count > MAX_RETRIES
+
+        retry
+      end
+    end
   end
 end
diff --git a/Library/Homebrew/api/cask.rb b/Library/Homebrew/api/cask.rb
index b7ec658bf2382..f0ed248cdf809 100644
--- a/Library/Homebrew/api/cask.rb
+++ b/Library/Homebrew/api/cask.rb
@@ -14,6 +14,18 @@ class << self
         def fetch(name)
           Homebrew::API.fetch "cask/#{name}.json"
         end
+
+        sig { returns(Hash) }
+        def all_casks
+          @all_casks ||= begin
+            json_casks = Homebrew::API.fetch_json_api_file "cask.json",
+                                                           target: HOMEBREW_CACHE_API/"cask.json"
+
+            json_casks.to_h do |json_cask|
+              [json_cask["token"], json_cask.except("token")]
+            end
+          end
+        end
       end
     end
   end
diff --git a/Library/Homebrew/api/formula.rb b/Library/Homebrew/api/formula.rb
index 0e62566220fe4..48ebf47fdc173 100644
--- a/Library/Homebrew/api/formula.rb
+++ b/Library/Homebrew/api/formula.rb
@@ -10,45 +10,16 @@ module Formula
       class << self
         extend T::Sig
 
-        MAX_RETRIES = 3
-
-        sig { returns(String) }
-        def formula_api_path
-          "formula"
-        end
-        alias generic_formula_api_path formula_api_path
-
-        sig { returns(String) }
-        def cached_formula_json_file
-          HOMEBREW_CACHE_API/"#{formula_api_path}.json"
-        end
-
         sig { params(name: String).returns(Hash) }
         def fetch(name)
-          Homebrew::API.fetch "#{formula_api_path}/#{name}.json"
+          Homebrew::API.fetch "formula/#{name}.json"
         end
 
         sig { returns(Hash) }
         def all_formulae
           @all_formulae ||= begin
-            retry_count = 0
-
-            url = "https://formulae.brew.sh/api/formula.json"
-            json_formulae = begin
-              curl_args = %W[--compressed --silent #{url}]
-              if cached_formula_json_file.exist? && !cached_formula_json_file.empty?
-                curl_args.prepend("--time-cond", cached_formula_json_file)
-              end
-              curl_download(*curl_args, to: cached_formula_json_file, max_time: 5)
-
-              JSON.parse(cached_formula_json_file.read)
-            rescue JSON::ParserError
-              cached_formula_json_file.unlink
-              retry_count += 1
-              odie "Cannot download non-corrupt #{url}!" if retry_count > MAX_RETRIES
-
-              retry
-            end
+            json_formulae = Homebrew::API.fetch_json_api_file "formula.json",
+                                                              target: HOMEBREW_CACHE_API/"formula.json"
 
             @all_aliases = {}
             json_formulae.to_h do |json_formula|
diff --git a/Library/Homebrew/cask/cask_loader.rb b/Library/Homebrew/cask/cask_loader.rb
index 28c53f7527bde..2e67869755999 100644
--- a/Library/Homebrew/cask/cask_loader.rb
+++ b/Library/Homebrew/cask/cask_loader.rb
@@ -186,6 +186,100 @@ def load(config:)
       end
     end
 
+    # Loads a cask from the JSON API.
+    class FromAPILoader
+      attr_reader :token, :path
+
+      FLIGHT_STANZAS = [:preflight, :postflight, :uninstall_preflight, :uninstall_postflight].freeze
+
+      def self.can_load?(ref)
+        Homebrew::API::Cask.all_casks.key? ref
+      end
+
+      def initialize(token)
+        @token = token
+        @path = CaskLoader.default_path(token)
+      end
+
+      def load(config:)
+        json_cask = Homebrew::API::Cask.all_casks[token]
+
+        if (bottle_tag = ::Utils::Bottles.tag.to_s.presence) &&
+           (variations = json_cask["variations"].presence) &&
+           (variation = variations[bottle_tag].presence)
+          json_cask = json_cask.merge(variation)
+        end
+
+        json_cask.deep_symbolize_keys!
+
+        # Use the cask-source API if there are any `*flight` blocks
+        if json_cask[:artifacts].any? { |artifact| FLIGHT_STANZAS.include?(artifact.keys.first) }
+          cask_source = Homebrew::API::CaskSource.fetch(token)
+          return FromContentLoader.new(cask_source).load(config: config)
+        end
+
+        Cask.new(token, source: cask_source, config: config) do
+          version json_cask[:version]
+
+          if json_cask[:sha256] == "no_check"
+            sha256 :no_check
+          else
+            sha256 json_cask[:sha256]
+          end
+
+          url json_cask[:url]
+          appcast json_cask[:appcast] if json_cask[:appcast].present?
+          json_cask[:name].each do |cask_name|
+            name cask_name
+          end
+          desc json_cask[:desc]
+          homepage json_cask[:homepage]
+
+          auto_updates json_cask[:auto_updates] if json_cask[:auto_updates].present?
+          conflicts_with(**json_cask[:conflicts_with]) if json_cask[:conflicts_with].present?
+
+          if json_cask[:depends_on].present?
+            dep_hash = json_cask[:depends_on].to_h do |dep_key, dep_value|
+              next [dep_key, dep_value] unless dep_key == :macos
+
+              dep_type = dep_value.keys.first
+              if dep_type == :==
+                version_symbols = dep_value[dep_type].map do |version|
+                  MacOSVersions::SYMBOLS.key(version) || version
+                end
+                next [dep_key, version_symbols]
+              end
+
+              version_symbol = dep_value[dep_type].first
+              version_symbol = MacOSVersions::SYMBOLS.key(version_symbol) || version_symbol
+              [dep_key, "#{dep_type} :#{version_symbol}"]
+            end.compact
+            depends_on(**dep_hash)
+          end
+
+          if json_cask[:container].present?
+            container_hash = json_cask[:container].to_h do |container_key, container_value|
+              next [container_key, container_value] unless container_key == :type
+
+              [container_key, container_value.to_sym]
+            end
+            container(**container_hash)
+          end
+
+          json_cask[:artifacts].each do |artifact|
+            key = artifact.keys.first
+            if FLIGHT_STANZAS.include?(key)
+              instance_eval(artifact[key])
+            else
+              send(key, *artifact[key])
+            end
+          end
+
+          caveats json_cask[:caveats] if json_cask[:caveats].present?
+        end
+      end
+    end
+
     # Pseudo-loader which raises an error when trying to load the corresponding cask.
     class NullLoader < FromPathLoader
       extend T::Sig
@@ -225,15 +319,15 @@ def self.for(ref, need_path: false)
         next unless loader_class.can_load?(ref)
 
         if loader_class == FromTapLoader && Homebrew::EnvConfig.install_from_api? &&
-           ref.start_with?("homebrew/cask/") && Homebrew::API::CaskSource.available?(ref)
-          return FromContentLoader.new(Homebrew::API::CaskSource.fetch(ref))
+           ref.start_with?("homebrew/cask/") && FromAPILoader.can_load?(ref)
+          return FromAPILoader.new(ref)
         end
 
         return loader_class.new(ref)
       end
 
       if Homebrew::EnvConfig.install_from_api? && !need_path && Homebrew::API::CaskSource.available?(ref)
-        return FromContentLoader.new(Homebrew::API::CaskSource.fetch(ref))
+        return FromAPILoader.new(ref)
       end
 
       return FromTapPathLoader.new(default_path(ref)) if FromTapPathLoader.can_load?(default_path(ref))
diff --git a/Library/Homebrew/cmd/update.sh b/Library/Homebrew/cmd/update.sh
index a171c450b46d7..c77a42845712f 100644
--- a/Library/Homebrew/cmd/update.sh
+++ b/Library/Homebrew/cmd/update.sh
@@ -754,28 +754,32 @@ EOS
   if [[ -n "${HOMEBREW_INSTALL_FROM_API}" ]]
   then
     mkdir -p "${HOMEBREW_CACHE}/api"
-    if [[ -f "${HOMEBREW_CACHE}/api/formula.json" ]]
-    then
-      INITIAL_JSON_BYTESIZE="$(wc -c "${HOMEBREW_CACHE}"/api/formula.json)"
-    fi
-    curl \
-      "${CURL_DISABLE_CURLRC_ARGS[@]}" \
-      --fail --compressed --silent --max-time 5 \
-      --location --remote-time --output "${HOMEBREW_CACHE}/api/formula.json" \
-      --time-cond "${HOMEBREW_CACHE}/api/formula.json" \
-      --user-agent "${HOMEBREW_USER_AGENT_CURL}" \
-      "https://formulae.brew.sh/api/formula.json"
-    curl_exit_code=$?
-    if [[ ${curl_exit_code} -eq 0 ]]
-    then
-      CURRENT_JSON_BYTESIZE="$(wc -c "${HOMEBREW_CACHE}"/api/formula.json)"
-      if [[ "${INITIAL_JSON_BYTESIZE}" != "${CURRENT_JSON_BYTESIZE}" ]]
+
+    for formula_or_cask in formula cask
+    do
+      if [[ -f "${HOMEBREW_CACHE}/api/${formula_or_cask}.json" ]]
       then
-        HOMEBREW_UPDATED="1"
+        INITIAL_JSON_BYTESIZE="$(wc -c "${HOMEBREW_CACHE}"/api/"${formula_or_cask}".json)"
       fi
-    else
-      echo "Failed to download formula.json!" >>"${update_failed_file}"
-    fi
+      curl \
+        "${CURL_DISABLE_CURLRC_ARGS[@]}" \
+        --fail --compressed --silent --max-time 5 \
+        --location --remote-time --output "${HOMEBREW_CACHE}/api/${formula_or_cask}.json" \
+        --time-cond "${HOMEBREW_CACHE}/api/${formula_or_cask}.json" \
+        --user-agent "${HOMEBREW_USER_AGENT_CURL}" \
+        "https://formulae.brew.sh/api/${formula_or_cask}.json"
+      curl_exit_code=$?
+      if [[ ${curl_exit_code} -eq 0 ]]
+      then
+        CURRENT_JSON_BYTESIZE="$(wc -c "${HOMEBREW_CACHE}"/api/"${formula_or_cask}".json)"
+        if [[ "${INITIAL_JSON_BYTESIZE}" != "${CURRENT_JSON_BYTESIZE}" ]]
+        then
+          HOMEBREW_UPDATED="1"
+        fi
+      else
+        echo "Failed to download ${formula_or_cask}.json!" >>"${update_failed_file}"
+      fi
+    done
   fi
 
   safe_cd "${HOMEBREW_REPOSITORY}"
diff --git a/Library/Homebrew/dev-cmd/bottle.rb b/Library/Homebrew/dev-cmd/bottle.rb
index 6104050fc7f68..73301317dd673 100644
--- a/Library/Homebrew/dev-cmd/bottle.rb
+++ b/Library/Homebrew/dev-cmd/bottle.rb
@@ -557,11 +557,10 @@ def bottle_formula(f, args:)
           "date"     => Pathname(filename.to_s).mtime.strftime("%F"),
           "tags"     => {
             bottle_tag.to_s => {
-              "filename"              => filename.url_encode,
-              "local_filename"        => filename.to_s,
-              "sha256"                => sha256,
-              "formulae_brew_sh_path" => Homebrew::API::Formula.formula_api_path,
-              "tab"                   => tab.to_bottle_hash,
+              "filename"       => filename.url_encode,
+              "local_filename" => filename.to_s,
+              "sha256"         => sha256,
+              "tab"            => tab.to_bottle_hash,
             },
           },
         },
diff --git a/Library/Homebrew/github_packages.rb b/Library/Homebrew/github_packages.rb
index 0527dcb401763..e50a1cbb62fdf 100644
--- a/Library/Homebrew/github_packages.rb
+++ b/Library/Homebrew/github_packages.rb
@@ -354,8 +354,7 @@ def upload_bottle(user, token, skopeo, formula_full_name, bottle_hash, keep_old:
 
       config_json_sha256, config_json_size = write_image_config(platform_hash, tar_sha256.hexdigest, blobs)
 
-      formulae_dir = tag_hash["formulae_brew_sh_path"]
-      documentation = "https://formulae.brew.sh/#{formulae_dir}/#{formula_name}" if formula_core_tap
+      documentation = "https://formulae.brew.sh/formula/#{formula_name}" if formula_core_tap
 
       descriptor_annotations_hash = {
         "org.opencontainers.image.ref.name" => tag,
diff --git a/Library/Homebrew/test/api/cask_spec.rb b/Library/Homebrew/test/api/cask_spec.rb
new file mode 100644
index 0000000000000..35c561b8f9c18
--- /dev/null
+++ b/Library/Homebrew/test/api/cask_spec.rb
@@ -0,0 +1,44 @@
+# typed: false
+# frozen_string_literal: true
+
+require "api"
+
+describe Homebrew::API::Cask do
+  let(:cache_dir) { mktmpdir }
+
+  before do
+    stub_const("Homebrew::API::HOMEBREW_CACHE_API", cache_dir)
+  end
+
+  def mock_curl_download(stdout:)
+    allow(Utils::Curl).to receive(:curl_download) do |*_args, **kwargs|
+      kwargs[:to].write stdout
+    end
+  end
+
+  describe "::all_casks" do
+    let(:casks_json) {
+      <<~EOS
+        [{
+          "token": "foo",
+          "url": "https://brew.sh/foo"
+        }, {
+          "token": "bar",
+          "url": "https://brew.sh/bar"
+        }]
+      EOS
+    }
+    let(:casks_hash) {
+      {
+        "foo" => { "url" => "https://brew.sh/foo" },
+        "bar" => { "url" => "https://brew.sh/bar" },
+      }
+    }
+
+    it "returns the expected cask JSON list" do
+      mock_curl_download stdout: casks_json
+      casks_output = described_class.all_casks
+      expect(casks_output).to eq casks_hash
+    end
+  end
+end
diff --git a/Library/Homebrew/test/api/formula_spec.rb b/Library/Homebrew/test/api/formula_spec.rb
new file mode 100644
index 0000000000000..38dbb57d5fe62
--- /dev/null
+++ b/Library/Homebrew/test/api/formula_spec.rb
@@ -0,0 +1,64 @@
+# typed: false
+# frozen_string_literal: true
+
+require "api"
+
+describe Homebrew::API::Formula do
+  let(:cache_dir) { mktmpdir }
+
+  before do
+    stub_const("Homebrew::API::HOMEBREW_CACHE_API", cache_dir)
+  end
+
+  def mock_curl_download(stdout:)
+    allow(Utils::Curl).to receive(:curl_download) do |*_args, **kwargs|
+      kwargs[:to].write stdout
+    end
+  end
+
+  describe "::all_formulae" do
+    let(:formulae_json) {
+      <<~EOS
+        [{
+          "name": "foo",
+          "url": "https://brew.sh/foo",
+          "aliases": ["foo-alias1", "foo-alias2"]
+        }, {
+          "name": "bar",
+          "url": "https://brew.sh/bar",
+          "aliases": ["bar-alias"]
+        }, {
+          "name": "baz",
+          "url": "https://brew.sh/baz",
+          "aliases": []
+        }]
+      EOS
+    }
+    let(:formulae_hash) {
+      {
+        "foo" => { "url" => "https://brew.sh/foo", "aliases" => ["foo-alias1", "foo-alias2"] },
+        "bar" => { "url" => "https://brew.sh/bar", "aliases" => ["bar-alias"] },
+        "baz" => { "url" => "https://brew.sh/baz", "aliases" => [] },
+      }
+    }
+    let(:formulae_aliases) {
+      {
+        "foo-alias1" => "foo",
+        "foo-alias2" => "foo",
+        "bar-alias"  => "bar",
+      }
+    }
+
+    it "returns the expected formula JSON list" do
+      mock_curl_download stdout: formulae_json
+      formulae_output = described_class.all_formulae
+      expect(formulae_output).to eq formulae_hash
+    end
+
+    it "returns the expected formula alias list" do
+      mock_curl_download stdout: formulae_json
+      aliases_output = described_class.all_aliases
+      expect(aliases_output).to eq formulae_aliases
+    end
+  end
+end
diff --git a/Library/Homebrew/test/api_spec.rb b/Library/Homebrew/test/api_spec.rb
index 6d70ef66269d8..ff695bfe7797f 100644
--- a/Library/Homebrew/test/api_spec.rb
+++ b/Library/Homebrew/test/api_spec.rb
@@ -7,12 +7,19 @@
   let(:text) { "foo" }
   let(:json) { '{"foo":"bar"}' }
   let(:json_hash) { JSON.parse(json) }
+  let(:json_invalid) { '{"foo":"bar"' }
 
   def mock_curl_output(stdout: "", success: true)
     curl_output = OpenStruct.new(stdout: stdout, success?: success)
     allow(Utils::Curl).to receive(:curl_output).and_return curl_output
   end
 
+  def mock_curl_download(stdout:)
+    allow(Utils::Curl).to receive(:curl_download) do |*_args, **kwargs|
+      kwargs[:to].write stdout
+    end
+  end
+
   describe "::fetch" do
     it "fetches a text file" do
       mock_curl_output stdout: text
@@ -36,4 +43,31 @@ def mock_curl_output(stdout: "", success: true)
       expect { described_class.fetch("baz.txt") }.to raise_error(ArgumentError, /Invalid JSON file/)
     end
   end
+
+  describe "::fetch_json_api_file" do
+    let!(:cache_dir) { mktmpdir }
+
+    before do
+      (cache_dir/"bar.json").write "tmp"
+    end
+
+    it "fetches a JSON file" do
+      mock_curl_download stdout: json
+      fetched_json = described_class.fetch_json_api_file("foo.json", target: cache_dir/"foo.json")
+      expect(fetched_json).to eq json_hash
+    end
+
+    it "updates an existing JSON file" do
+      mock_curl_download stdout: json
+      fetched_json = described_class.fetch_json_api_file("bar.json", target: cache_dir/"bar.json")
+      expect(fetched_json).to eq json_hash
+    end
+
+    it "raises an error if the JSON file is invalid" do
+      mock_curl_download stdout: json_invalid
+      expect {
+        described_class.fetch_json_api_file("baz.json", target: cache_dir/"baz.json")
+      }.to raise_error(SystemExit)
+    end
+  end
 end