diff --git a/esphome/codegen.py b/esphome/codegen.py
index 5debb52b4e..3dfec65f23 100644
--- a/esphome/codegen.py
+++ b/esphome/codegen.py
@@ -64,7 +64,6 @@ from esphome.cpp_types import (  # noqa: F401
     Application,
     Component,
     ComponentPtr,
-    Controller,
     EntityBase,
     EntityCategory,
     ESPTime,
diff --git a/esphome/components/api/__init__.py b/esphome/components/api/__init__.py
index 854bceecfa..2291dc54f8 100644
--- a/esphome/components/api/__init__.py
+++ b/esphome/components/api/__init__.py
@@ -81,7 +81,7 @@ def AUTO_LOAD(config: ConfigType) -> list[str]:
 
 
 api_ns = cg.esphome_ns.namespace("api")
-APIServer = api_ns.class_("APIServer", cg.Component, cg.Controller)
+APIServer = api_ns.class_("APIServer", cg.Component)
 HomeAssistantServiceCallAction = api_ns.class_(
     "HomeAssistantServiceCallAction", automation.Action
 )
@@ -462,8 +462,7 @@ async def to_code(config: ConfigType) -> None:
     var = cg.new_Pvariable(config[CONF_ID])
     await cg.register_component(var, config)
 
-    # Track controller registration for StaticVector sizing
-    CORE.register_controller()
+    CORE.register_controller(var)
 
     # Request a log listener slot for API log streaming
     request_log_listener()
diff --git a/esphome/components/api/api_server.cpp b/esphome/components/api/api_server.cpp
index 310cdcf67b..2a89d31a74 100644
--- a/esphome/components/api/api_server.cpp
+++ b/esphome/components/api/api_server.cpp
@@ -5,7 +5,6 @@
 #include "api_connection.h"
 #include "esphome/components/network/util.h"
 #include "esphome/core/application.h"
-#include "esphome/core/controller_registry.h"
 #include "esphome/core/defines.h"
 #include "esphome/core/hal.h"
 #include "esphome/core/log.h"
@@ -61,8 +60,6 @@ void APIServer::socket_failed_(const LogString *msg) {
 }
 
 void APIServer::setup() {
-  ControllerRegistry::register_controller(this);
-
 #ifdef USE_API_NOISE
   // Always reserve the slot: flash preferences are positional on esp8266, so
   // a yaml key build must keep the layout of a runtime key build
diff --git a/esphome/components/api/api_server.h b/esphome/components/api/api_server.h
index b8a71c93e7..49cf77ca5a 100644
--- a/esphome/components/api/api_server.h
+++ b/esphome/components/api/api_server.h
@@ -14,7 +14,7 @@
 #include "esphome/components/socket/socket.h"
 #include "esphome/core/automation.h"
 #include "esphome/core/component.h"
-#include "esphome/core/controller.h"
+#include "esphome/core/entity_includes.h"
 #include "esphome/core/log.h"
 #include "esphome/core/string_ref.h"
 #ifdef USE_PROVISIONING
@@ -49,8 +49,7 @@ struct SavedNoisePsk {
 bool load_saved_noise_psk(noise::psk_t &out);
 #endif
 
-class APIServer final : public Component,
-                        public Controller
+class APIServer final : public Component
 #ifdef USE_CAMERA
     ,
                         public camera::CameraListener
@@ -94,58 +93,58 @@ class APIServer final : public Component,
 
   void handle_disconnect(APIConnection *conn);
 #ifdef USE_BINARY_SENSOR
-  void on_binary_sensor_update(binary_sensor::BinarySensor *obj) override;
+  void on_binary_sensor_update(binary_sensor::BinarySensor *obj);
 #endif
 #ifdef USE_COVER
-  void on_cover_update(cover::Cover *obj) override;
+  void on_cover_update(cover::Cover *obj);
 #endif
 #ifdef USE_FAN
-  void on_fan_update(fan::Fan *obj) override;
+  void on_fan_update(fan::Fan *obj);
 #endif
 #ifdef USE_LIGHT
-  void on_light_update(light::LightState *obj) override;
+  void on_light_update(light::LightState *obj);
 #endif
 #ifdef USE_SENSOR
-  void on_sensor_update(sensor::Sensor *obj) override;
+  void on_sensor_update(sensor::Sensor *obj);
 #endif
 #ifdef USE_SWITCH
-  void on_switch_update(switch_::Switch *obj) override;
+  void on_switch_update(switch_::Switch *obj);
 #endif
 #ifdef USE_TEXT_SENSOR
-  void on_text_sensor_update(text_sensor::TextSensor *obj) override;
+  void on_text_sensor_update(text_sensor::TextSensor *obj);
 #endif
 #ifdef USE_CLIMATE
-  void on_climate_update(climate::Climate *obj) override;
+  void on_climate_update(climate::Climate *obj);
 #endif
 #ifdef USE_NUMBER
-  void on_number_update(number::Number *obj) override;
+  void on_number_update(number::Number *obj);
 #endif
 #ifdef USE_DATETIME_DATE
-  void on_date_update(datetime::DateEntity *obj) override;
+  void on_date_update(datetime::DateEntity *obj);
 #endif
 #ifdef USE_DATETIME_TIME
-  void on_time_update(datetime::TimeEntity *obj) override;
+  void on_time_update(datetime::TimeEntity *obj);
 #endif
 #ifdef USE_DATETIME_DATETIME
-  void on_datetime_update(datetime::DateTimeEntity *obj) override;
+  void on_datetime_update(datetime::DateTimeEntity *obj);
 #endif
 #ifdef USE_TEXT
-  void on_text_update(text::Text *obj) override;
+  void on_text_update(text::Text *obj);
 #endif
 #ifdef USE_SELECT
-  void on_select_update(select::Select *obj) override;
+  void on_select_update(select::Select *obj);
 #endif
 #ifdef USE_LOCK
-  void on_lock_update(lock::Lock *obj) override;
+  void on_lock_update(lock::Lock *obj);
 #endif
 #ifdef USE_VALVE
-  void on_valve_update(valve::Valve *obj) override;
+  void on_valve_update(valve::Valve *obj);
 #endif
 #ifdef USE_MEDIA_PLAYER
-  void on_media_player_update(media_player::MediaPlayer *obj) override;
+  void on_media_player_update(media_player::MediaPlayer *obj);
 #endif
 #ifdef USE_WATER_HEATER
-  void on_water_heater_update(water_heater::WaterHeater *obj) override;
+  void on_water_heater_update(water_heater::WaterHeater *obj);
 #endif
 #ifdef USE_API_HOMEASSISTANT_SERVICES
   void send_homeassistant_action(const HomeassistantActionRequest &call);
@@ -188,13 +187,13 @@ class APIServer final : public Component,
 #endif
 
 #ifdef USE_ALARM_CONTROL_PANEL
-  void on_alarm_control_panel_update(alarm_control_panel::AlarmControlPanel *obj) override;
+  void on_alarm_control_panel_update(alarm_control_panel::AlarmControlPanel *obj);
 #endif
 #ifdef USE_EVENT
-  void on_event(event::Event *obj) override;
+  void on_event(event::Event *obj);
 #endif
 #ifdef USE_UPDATE
-  void on_update(update::UpdateEntity *obj) override;
+  void on_update(update::UpdateEntity *obj);
 #endif
 #ifdef USE_ZWAVE_PROXY
   void on_zwave_proxy_request(const ZWaveProxyRequest &msg);
diff --git a/esphome/components/api/subscribe_state.h b/esphome/components/api/subscribe_state.h
index 6b1ae9651d..36e96e1081 100644
--- a/esphome/components/api/subscribe_state.h
+++ b/esphome/components/api/subscribe_state.h
@@ -4,7 +4,6 @@
 #ifdef USE_API
 #include "esphome/core/component.h"
 #include "esphome/core/component_iterator.h"
-#include "esphome/core/controller.h"
 namespace esphome::api {
 
 class APIConnection;
diff --git a/esphome/components/prometheus/prometheus_handler.h b/esphome/components/prometheus/prometheus_handler.h
index 5574039e41..9dcbf7e686 100644
--- a/esphome/components/prometheus/prometheus_handler.h
+++ b/esphome/components/prometheus/prometheus_handler.h
@@ -6,8 +6,8 @@
 
 #include "esphome/components/web_server_base/web_server_base.h"
 #include "esphome/core/component.h"
-#include "esphome/core/controller.h"
 #include "esphome/core/entity_base.h"
+#include "esphome/core/entity_includes.h"
 #include "esphome/core/progmem.h"
 #ifdef USE_CLIMATE
 #include "esphome/core/log.h"
diff --git a/esphome/components/web_server/__init__.py b/esphome/components/web_server/__init__.py
index 2459163786..3ec365cf38 100644
--- a/esphome/components/web_server/__init__.py
+++ b/esphome/components/web_server/__init__.py
@@ -62,7 +62,7 @@ DEFAULT_PORT = 80
 
 
 web_server_ns = cg.esphome_ns.namespace("web_server")
-WebServer = web_server_ns.class_("WebServer", cg.Component, cg.Controller)
+WebServer = web_server_ns.class_("WebServer", cg.Component)
 
 sorting_groups = {}
 
@@ -378,8 +378,7 @@ async def to_code(config: ConfigType) -> None:
     var = cg.new_Pvariable(config[CONF_ID], paren)
     await cg.register_component(var, config)
 
-    # Track controller registration for StaticVector sizing
-    CORE.register_controller()
+    CORE.register_controller(var)
 
     version = config[CONF_VERSION]
 
diff --git a/esphome/components/web_server/web_server.cpp b/esphome/components/web_server/web_server.cpp
index 49943f8a71..4906a2050a 100644
--- a/esphome/components/web_server/web_server.cpp
+++ b/esphome/components/web_server/web_server.cpp
@@ -5,7 +5,6 @@
 #include "esphome/components/network/util.h"
 #include "esphome/core/application.h"
 #include "esphome/core/defines.h"
-#include "esphome/core/controller_registry.h"
 #include "esphome/core/entity_base.h"
 #include "esphome/core/helpers.h"
 #include "esphome/core/log.h"
@@ -365,7 +364,6 @@ json::SerializationBuffer<> WebServer::get_config_json() {
 }
 
 void WebServer::setup() {
-  ControllerRegistry::register_controller(this);
   this->base_->init();
 
 #ifdef USE_LOGGER
diff --git a/esphome/components/web_server/web_server.h b/esphome/components/web_server/web_server.h
index 3e50eeeec0..3236ccfd3c 100644
--- a/esphome/components/web_server/web_server.h
+++ b/esphome/components/web_server/web_server.h
@@ -6,8 +6,8 @@
 #include "esphome/components/web_server_base/web_server_base.h"
 #ifdef USE_WEBSERVER
 #include "esphome/core/component.h"
-#include "esphome/core/controller.h"
 #include "esphome/core/entity_base.h"
+#include "esphome/core/entity_includes.h"
 #include "esphome/core/progmem.h"
 #ifdef USE_LOGGER
 #include "esphome/components/logger/logger.h"
@@ -187,7 +187,7 @@ class DeferredUpdateEventSourceList final : public std::list<DeferredUpdateEvent
  * under the '/light/...', '/sensor/...', ... URLs. A full documentation for this API
  * can be found under https://esphome.io/web-api/.
  */
-class WebServer final : public Controller, public Component, public AsyncWebHandler {
+class WebServer final : public Component, public AsyncWebHandler {
 #if !defined(USE_ESP32) && defined(USE_ARDUINO)
   friend class DeferredUpdateEventSourceList;
 #endif
@@ -292,7 +292,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_SENSOR
-  void on_sensor_update(sensor::Sensor *obj) override;
+  void on_sensor_update(sensor::Sensor *obj);
   /// Handle a sensor request under '/sensor/<id>'.
   void handle_sensor_request(AsyncWebServerRequest *request, const UrlMatch &match);
 
@@ -301,7 +301,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_SWITCH
-  void on_switch_update(switch_::Switch *obj) override;
+  void on_switch_update(switch_::Switch *obj);
 
   /// Handle a switch request under '/switch/<id>/</turn_on/turn_off/toggle>'.
   void handle_switch_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -319,7 +319,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_BINARY_SENSOR
-  void on_binary_sensor_update(binary_sensor::BinarySensor *obj) override;
+  void on_binary_sensor_update(binary_sensor::BinarySensor *obj);
 
   /// Handle a binary sensor request under '/binary_sensor/<id>'.
   void handle_binary_sensor_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -329,7 +329,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_FAN
-  void on_fan_update(fan::Fan *obj) override;
+  void on_fan_update(fan::Fan *obj);
 
   /// Handle a fan request under '/fan/<id>/</turn_on/turn_off/toggle>'.
   void handle_fan_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -339,7 +339,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_LIGHT
-  void on_light_update(light::LightState *obj) override;
+  void on_light_update(light::LightState *obj);
 
   /// Handle a light request under '/light/<id>/</turn_on/turn_off/toggle>'.
   void handle_light_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -349,7 +349,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_TEXT_SENSOR
-  void on_text_sensor_update(text_sensor::TextSensor *obj) override;
+  void on_text_sensor_update(text_sensor::TextSensor *obj);
 
   /// Handle a text sensor request under '/text_sensor/<id>'.
   void handle_text_sensor_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -359,7 +359,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_COVER
-  void on_cover_update(cover::Cover *obj) override;
+  void on_cover_update(cover::Cover *obj);
 
   /// Handle a cover request under '/cover/<id>/<open/close/stop/set>'.
   void handle_cover_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -369,7 +369,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_NUMBER
-  void on_number_update(number::Number *obj) override;
+  void on_number_update(number::Number *obj);
   /// Handle a number request under '/number/<id>'.
   void handle_number_request(AsyncWebServerRequest *request, const UrlMatch &match);
 
@@ -378,7 +378,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_DATETIME_DATE
-  void on_date_update(datetime::DateEntity *obj) override;
+  void on_date_update(datetime::DateEntity *obj);
   /// Handle a date request under '/date/<id>'.
   void handle_date_request(AsyncWebServerRequest *request, const UrlMatch &match);
 
@@ -387,7 +387,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_DATETIME_TIME
-  void on_time_update(datetime::TimeEntity *obj) override;
+  void on_time_update(datetime::TimeEntity *obj);
   /// Handle a time request under '/time/<id>'.
   void handle_time_request(AsyncWebServerRequest *request, const UrlMatch &match);
 
@@ -396,7 +396,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_DATETIME_DATETIME
-  void on_datetime_update(datetime::DateTimeEntity *obj) override;
+  void on_datetime_update(datetime::DateTimeEntity *obj);
   /// Handle a datetime request under '/datetime/<id>'.
   void handle_datetime_request(AsyncWebServerRequest *request, const UrlMatch &match);
 
@@ -405,7 +405,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_TEXT
-  void on_text_update(text::Text *obj) override;
+  void on_text_update(text::Text *obj);
   /// Handle a text input request under '/text/<id>'.
   void handle_text_request(AsyncWebServerRequest *request, const UrlMatch &match);
 
@@ -414,7 +414,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_SELECT
-  void on_select_update(select::Select *obj) override;
+  void on_select_update(select::Select *obj);
   /// Handle a select request under '/select/<id>'.
   void handle_select_request(AsyncWebServerRequest *request, const UrlMatch &match);
 
@@ -423,7 +423,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_CLIMATE
-  void on_climate_update(climate::Climate *obj) override;
+  void on_climate_update(climate::Climate *obj);
   /// Handle a climate request under '/climate/<id>'.
   void handle_climate_request(AsyncWebServerRequest *request, const UrlMatch &match);
 
@@ -432,7 +432,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_LOCK
-  void on_lock_update(lock::Lock *obj) override;
+  void on_lock_update(lock::Lock *obj);
 
   /// Handle a lock request under '/lock/<id>/</lock/unlock/open>'.
   void handle_lock_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -442,7 +442,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_VALVE
-  void on_valve_update(valve::Valve *obj) override;
+  void on_valve_update(valve::Valve *obj);
 
   /// Handle a valve request under '/valve/<id>/<open/close/stop/set>'.
   void handle_valve_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -452,7 +452,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_ALARM_CONTROL_PANEL
-  void on_alarm_control_panel_update(alarm_control_panel::AlarmControlPanel *obj) override;
+  void on_alarm_control_panel_update(alarm_control_panel::AlarmControlPanel *obj);
 
   /// Handle a alarm_control_panel request under '/alarm_control_panel/<id>'.
   void handle_alarm_control_panel_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -462,7 +462,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_WATER_HEATER
-  void on_water_heater_update(water_heater::WaterHeater *obj) override;
+  void on_water_heater_update(water_heater::WaterHeater *obj);
 
   /// Handle a water_heater request under '/water_heater/<id>/<mode/set>'.
   void handle_water_heater_request(AsyncWebServerRequest *request, const UrlMatch &match);
@@ -484,8 +484,13 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
   static json::SerializationBuffer<> radio_frequency_all_json_generator(WebServer *web_server, void *source);
 #endif
 
+#ifdef USE_MEDIA_PLAYER
+  // Not exposed over HTTP; the stub only satisfies ControllerContract
+  void on_media_player_update(media_player::MediaPlayer *) {}
+#endif
+
 #ifdef USE_EVENT
-  void on_event(event::Event *obj) override;
+  void on_event(event::Event *obj);
 
   static json::SerializationBuffer<> event_state_json_generator(WebServer *web_server, void *source);
   static json::SerializationBuffer<> event_all_json_generator(WebServer *web_server, void *source);
@@ -495,7 +500,7 @@ class WebServer final : public Controller, public Component, public AsyncWebHand
 #endif
 
 #ifdef USE_UPDATE
-  void on_update(update::UpdateEntity *obj) override;
+  void on_update(update::UpdateEntity *obj);
 
   /// Handle a update request under '/update/<id>'.
   void handle_update_request(AsyncWebServerRequest *request, const UrlMatch &match);
diff --git a/esphome/core/__init__.py b/esphome/core/__init__.py
index 5fcad90a81..fb75285081 100644
--- a/esphome/core/__init__.py
+++ b/esphome/core/__init__.py
@@ -52,8 +52,8 @@ if TYPE_CHECKING:
 
 _LOGGER = logging.getLogger(__name__)
 
-# Key for tracking controller count in CORE.data for ControllerRegistry StaticVector sizing
-KEY_CONTROLLER_REGISTRY_COUNT = "controller_registry_count"
+# Key for the controllers (APIServer, WebServer) that receive entity state updates
+KEY_CONTROLLER_REGISTRY_CONTROLLERS = "controller_registry_controllers"
 
 # CORE.data key for the "is_rp2040 deprecation warning already fired this
 # run" flag. Mirrors the ``cv.only_on_rp2040`` dedupe pattern; cleared
@@ -1209,10 +1209,9 @@ class EsphomeCore:
         if not self.platform_counts[platform_name]:
             self.platform_counts[platform_name] = 1
 
-    def register_controller(self) -> None:
-        """Track registration of a Controller for ControllerRegistry StaticVector sizing."""
-        controller_count = self.data.setdefault(KEY_CONTROLLER_REGISTRY_COUNT, 0)
-        self.data[KEY_CONTROLLER_REGISTRY_COUNT] = controller_count + 1
+    def register_controller(self, controller: "MockObj") -> None:
+        """Register a controller that receives every entity state update."""
+        self.data.setdefault(KEY_CONTROLLER_REGISTRY_CONTROLLERS, []).append(controller)
 
     @property
     def cpp_main_section(self):
diff --git a/esphome/core/component_iterator.h b/esphome/core/component_iterator.h
index fac09e9e14..3c11d4a880 100644
--- a/esphome/core/component_iterator.h
+++ b/esphome/core/component_iterator.h
@@ -1,7 +1,7 @@
 #pragma once
 
 #include "esphome/core/component.h"
-#include "esphome/core/controller.h"
+#include "esphome/core/entity_includes.h"
 #include "esphome/core/helpers.h"
 
 #ifdef USE_CAMERA
diff --git a/esphome/core/config.py b/esphome/core/config.py
index 051a136aab..4d3fb83312 100644
--- a/esphome/core/config.py
+++ b/esphome/core/config.py
@@ -46,7 +46,7 @@ from esphome.const import (
 )
 from esphome.core import (
     CORE,
-    KEY_CONTROLLER_REGISTRY_COUNT,
+    KEY_CONTROLLER_REGISTRY_CONTROLLERS,
     CoroPriority,
     coroutine_with_priority,
 )
@@ -674,12 +674,22 @@ async def _add_platform_defines() -> None:
 
 
 @coroutine_with_priority(CoroPriority.FINAL)
-async def _add_controller_registry_define() -> None:
-    # Generate StaticVector size for ControllerRegistry
-    controller_count = CORE.data.get(KEY_CONTROLLER_REGISTRY_COUNT, 0)
-    if controller_count > 0:
-        cg.add_define("USE_CONTROLLER_REGISTRY")
-        cg.add_define("CONTROLLER_REGISTRY_MAX", controller_count)
+async def _add_controller_registry_dispatch() -> None:
+    # controller_dispatch.h defines ControllerRegistry::notify_*() as direct
+    # calls on the controllers returned by esphome_controllers(), emitted as
+    #   static auto esphome_controllers() { return std::tuple{a, b}; }
+    controllers = CORE.data.get(KEY_CONTROLLER_REGISTRY_CONTROLLERS)
+    if not controllers:
+        return
+    cg.add_define("USE_CONTROLLER_REGISTRY")
+    controllers = cg.ArrayInitializer(*controllers)
+    cg.add_global(cg.RawStatement("#include <tuple>"))
+    cg.add_global(
+        cg.RawStatement(
+            f"static auto esphome_controllers() {{ return std::tuple{controllers}; }}"
+        )
+    )
+    cg.add_global(cg.RawStatement('#include "esphome/core/controller_dispatch.h"'))
 
 
 @coroutine_with_priority(CoroPriority.FINAL)
@@ -755,7 +765,7 @@ async def to_code(config: ConfigType) -> None:
     )
 
     CORE.add_job(_add_platform_defines)
-    CORE.add_job(_add_controller_registry_define)
+    CORE.add_job(_add_controller_registry_dispatch)
     CORE.add_job(_add_looping_components)
 
     CORE.add_job(_add_automations, config)
diff --git a/esphome/core/controller.h b/esphome/core/controller.h
deleted file mode 100644
index 09975b465f..0000000000
--- a/esphome/core/controller.h
+++ /dev/null
@@ -1,19 +0,0 @@
-#pragma once
-
-#include "esphome/core/entity_includes.h"
-
-namespace esphome {
-
-class Controller {
- public:
-// Controller virtual methods (generated from entity_types.h)
-// NOLINTBEGIN(bugprone-macro-parentheses)
-#define ENTITY_TYPE_(type, singular, plural, count, upper)  // no controller callback
-#define ENTITY_CONTROLLER_TYPE_(type, singular, plural, count, upper, callback) virtual void on_##callback(type *obj){};
-#include "esphome/core/entity_types.h"
-#undef ENTITY_TYPE_
-#undef ENTITY_CONTROLLER_TYPE_
-  // NOLINTEND(bugprone-macro-parentheses)
-};
-
-}  // namespace esphome
diff --git a/esphome/core/controller_dispatch.h b/esphome/core/controller_dispatch.h
new file mode 100644
index 0000000000..fc6a03556d
--- /dev/null
+++ b/esphome/core/controller_dispatch.h
@@ -0,0 +1,50 @@
+#pragma once
+
+// Included once by the generated main.cpp, after it returns the registered controllers as a tuple:
+//
+//   static auto esphome_controllers() { return std::tuple{api_apiserver_id, web_server_webserver_id}; }
+//   #include "esphome/core/controller_dispatch.h"
+//
+// Defines ControllerRegistry::notify_*() as direct calls on those controllers. Excluded from
+// esphome.h and the clang-tidy all-headers file, so nothing else includes it.
+
+#include <tuple>
+#include <type_traits>
+
+#include "esphome/core/controller_registry.h"
+
+namespace esphome {
+
+// NOLINTBEGIN(bugprone-macro-parentheses)
+
+/// A controller provides a plain on_*_update() member for every entity type in the build.
+template<typename T>
+concept ControllerContract = requires(T &controller) {
+  controller;  // keeps the requirement list non-empty when no entity type has a callback
+#define ENTITY_TYPE_(type, singular, plural, count, upper)  // no controller callback
+#define ENTITY_CONTROLLER_TYPE_(type, singular, plural, count, upper, callback) \
+  controller.on_##callback(static_cast<type *>(nullptr));
+#include "esphome/core/entity_types.h"
+#undef ENTITY_TYPE_
+#undef ENTITY_CONTROLLER_TYPE_
+};
+
+template<typename... Controllers> constexpr bool controllers_satisfy_contract(std::tuple<Controllers...> *) {
+  return (ControllerContract<std::remove_pointer_t<Controllers>> && ...);
+}
+static_assert(controllers_satisfy_contract(static_cast<decltype(esphome_controllers()) *>(nullptr)),
+              "A registered controller is missing an on_*_update() callback for an entity type in this build "
+              "(ControllerContract in esphome/core/controller_dispatch.h)");
+
+#define ENTITY_TYPE_(type, singular, plural, count, upper)  // no controller callback
+#define ENTITY_CONTROLLER_TYPE_(type, singular, plural, count, upper, callback) \
+  void ControllerRegistry::notify_##callback(type *obj) { \
+    std::apply([obj](auto *...controller) { (controller->on_##callback(obj), ...); }, esphome_controllers()); \
+  }
+#include "esphome/core/entity_types.h"
+#undef ENTITY_TYPE_
+#undef ENTITY_CONTROLLER_TYPE_
+
+// NOLINTEND(bugprone-macro-parentheses)
+
+}  // namespace esphome
diff --git a/esphome/core/controller_registry.cpp b/esphome/core/controller_registry.cpp
deleted file mode 100644
index 907e0f923d..0000000000
--- a/esphome/core/controller_registry.cpp
+++ /dev/null
@@ -1,11 +0,0 @@
-#include "esphome/core/controller_registry.h"
-
-#ifdef USE_CONTROLLER_REGISTRY
-
-namespace esphome {
-
-StaticVector<Controller *, CONTROLLER_REGISTRY_MAX> ControllerRegistry::controllers;
-
-}  // namespace esphome
-
-#endif  // USE_CONTROLLER_REGISTRY
diff --git a/esphome/core/controller_registry.h b/esphome/core/controller_registry.h
index c6113116ff..8b1b6c7f9d 100644
--- a/esphome/core/controller_registry.h
+++ b/esphome/core/controller_registry.h
@@ -5,37 +5,18 @@
 #ifdef USE_CONTROLLER_REGISTRY
 
 #include "esphome/core/entity_includes.h"
-#include "esphome/core/helpers.h"
 
 namespace esphome {
 
-class Controller;
-
-/** Global registry for Controllers to receive entity state updates.
+/** Fan-out of entity state updates to the controllers (APIServer, WebServer).
  *
- * This singleton registry allows Controllers (APIServer, WebServer) to receive
- * entity state change notifications without storing per-entity callbacks.
- *
- * Instead of each entity maintaining controller callbacks (32 bytes overhead per entity),
- * entities call ControllerRegistry::notify_*_update() which iterates the small list
- * of registered controllers (typically 2: API and WebServer).
- *
- * Each notify method directly iterates controllers and calls the virtual method,
- * avoiding function pointer indirection for minimal dispatch overhead.
- *
- * Memory savings: 32 bytes per entity (2 controllers × 16 bytes std::function overhead)
- * Typical config (25 entities): ~780 bytes saved
- * Large config (80 entities): ~2,540 bytes saved
+ * Entities call ControllerRegistry::notify_*_update() instead of holding
+ * per-entity controller callbacks. The functions are only declared here;
+ * controller_dispatch.h, included by the generated main.cpp, defines them as
+ * direct calls on the controllers registered through CORE.register_controller().
  */
 class ControllerRegistry {
  public:
-  /** Register a controller to receive entity state updates.
-   *
-   * Controllers should call this in their setup() method.
-   * Typically only APIServer and WebServer register.
-   */
-  static void register_controller(Controller *controller) { controllers.push_back(controller); }
-
 // Notify method declarations (generated from entity_types.h)
 // NOLINTBEGIN(bugprone-macro-parentheses)
 #define ENTITY_TYPE_(type, singular, plural, count, upper)  // no controller callback
@@ -45,38 +26,8 @@ class ControllerRegistry {
 #undef ENTITY_TYPE_
 #undef ENTITY_CONTROLLER_TYPE_
   // NOLINTEND(bugprone-macro-parentheses)
-
- protected:
-  static StaticVector<Controller *, CONTROLLER_REGISTRY_MAX> controllers;
 };
 
 }  // namespace esphome
 
-// Include controller.h AFTER the class definition so notify methods can be
-// defined inline. This is safe because controller_registry.h is only ever
-// included from .cpp files, never from other headers.
-#include "esphome/core/controller.h"
-
-namespace esphome {
-
-// Inline notify methods — each is a tiny loop over 1-2 controllers.
-// Defining them here (rather than in controller_registry.cpp) allows the
-// compiler to inline them into the single call site in each entity's
-// notify_frontend_(), eliminating an unnecessary function-call frame.
-
-// NOLINTBEGIN(bugprone-macro-parentheses)
-#define ENTITY_TYPE_(type, singular, plural, count, upper)  // no controller callback
-#define ENTITY_CONTROLLER_TYPE_(type, singular, plural, count, upper, callback) \
-  inline void ControllerRegistry::notify_##callback(type *obj) { \
-    for (auto *controller : controllers) { \
-      controller->on_##callback(obj); \
-    } \
-  }
-#include "esphome/core/entity_types.h"
-#undef ENTITY_TYPE_
-#undef ENTITY_CONTROLLER_TYPE_
-// NOLINTEND(bugprone-macro-parentheses)
-
-}  // namespace esphome
-
 #endif  // USE_CONTROLLER_REGISTRY
diff --git a/esphome/core/defines.h b/esphome/core/defines.h
index 7bc08ea577..e1ae1d5fb6 100644
--- a/esphome/core/defines.h
+++ b/esphome/core/defines.h
@@ -629,7 +629,6 @@
 #define USE_DASHBOARD_IMPORT
 
 // Default counts for static analysis
-#define CONTROLLER_REGISTRY_MAX 2
 #define ESPHOME_AREA_COUNT 10
 #define ESPHOME_COMPONENT_COUNT 50
 #define ESPHOME_DEVICE_COUNT 10
diff --git a/esphome/cpp_types.py b/esphome/cpp_types.py
index 45d6559b3f..04892f5fea 100644
--- a/esphome/cpp_types.py
+++ b/esphome/cpp_types.py
@@ -37,7 +37,6 @@ optional = global_ns.namespace("std").class_("optional")
 arduino_json_ns = global_ns.namespace("ArduinoJson")
 JsonObject = arduino_json_ns.class_("JsonObject")
 JsonObjectConst = arduino_json_ns.class_("JsonObjectConst")
-Controller = esphome_ns.class_("Controller")
 GPIOPin = esphome_ns.class_("GPIOPin")
 InternalGPIOPin = esphome_ns.class_("InternalGPIOPin", GPIOPin)
 gpio_ns = esphome_ns.namespace("gpio")
diff --git a/esphome/writer.py b/esphome/writer.py
index 0b9e7669ef..9ab5d644c5 100644
--- a/esphome/writer.py
+++ b/esphome/writer.py
@@ -211,6 +211,16 @@ VERSION_H_TARGET = "esphome/core/version.h"
 BUILD_INFO_DATA_H_TARGET = "esphome/core/build_info_data.h"
 BUILD_INFO_DATA_CPP_TARGET = "esphome/core/build_info_data.cpp"
 ENTITY_TYPES_H_TARGET = "esphome/core/entity_types.h"
+# Headers that must not be included bare from esphome.h or the clang-tidy
+# all-headers file: X-macro files, headers main.cpp includes itself, and
+# deprecated headers that only resolve when their new component is loaded.
+ESPHOME_H_EXCLUDE = {
+    Path(ENTITY_TYPES_H_TARGET),
+    # main.cpp includes it after defining esphome_controllers()
+    Path("esphome/core/controller_dispatch.h"),
+    # moved to components/ring_buffer/, removed in 2026.11.0
+    Path("esphome/core/ring_buffer.h"),
+}
 ESPHOME_README_TXT = """
 THIS DIRECTORY IS AUTO-GENERATED, DO NOT MODIFY
 
@@ -236,20 +246,9 @@ def copy_src_tree():
     source_files_l.sort()
 
     # Build #include list for esphome.h
-    # X-macro files are included multiple times with different macro definitions
-    # and must not be included bare in esphome.h
-    # Deprecated headers that re-export from a relocated component must not be
-    # auto-included, since their #include of the new path only resolves when the
-    # new component is loaded by a consumer.
-    esphome_h_exclude = {
-        Path(ENTITY_TYPES_H_TARGET),
-        Path(
-            "esphome/core/ring_buffer.h"
-        ),  # moved to components/ring_buffer/, removed in 2026.11.0
-    }
     include_l = []
     for target, _ in source_files_l:
-        if target.suffix in HEADER_FILE_EXTENSIONS and target not in esphome_h_exclude:
+        if target.suffix in HEADER_FILE_EXTENSIONS and target not in ESPHOME_H_EXCLUDE:
             include_l.append(f'#include "{target}"')
     include_l.append("")
     include_s = "\n".join(include_l)
diff --git a/script/helpers.py b/script/helpers.py
index a8a237118f..fb2c964bdd 100644
--- a/script/helpers.py
+++ b/script/helpers.py
@@ -429,11 +429,9 @@ def build_all_include(header_files: list[str] | None = None) -> None:
             if line
         ]
 
-    from esphome.writer import ENTITY_TYPES_H_TARGET
+    from esphome.writer import ESPHOME_H_EXCLUDE
 
-    # X-macro files are included multiple times with different macro definitions
-    # and must not be included bare in the all-include header
-    exclude = {ENTITY_TYPES_H_TARGET}
+    exclude = {path.as_posix() for path in ESPHOME_H_EXCLUDE}
     headers = [f'#include "{h}"' for h in header_files if h not in exclude]
     headers.sort()
     headers.append("")
diff --git a/tests/components/api/__init__.py b/tests/components/api/__init__.py
index 2aa558726c..a5e3731c75 100644
--- a/tests/components/api/__init__.py
+++ b/tests/components/api/__init__.py
@@ -1,5 +1,4 @@
 import esphome.codegen as cg
-from esphome.core import CORE
 from tests.testing_helpers import ComponentManifestOverride
 
 
@@ -12,6 +11,5 @@ def override_manifest(manifest: ComponentManifestOverride) -> None:
         cg.add_define("API_MAX_SEND_QUEUE", 8)
         cg.add_define("MAX_API_CONNECTIONS", 1)
         cg.add_define("USE_SOCKET_IMPL_BSD_SOCKETS")
-        CORE.register_controller()  # api_server registers with the controller registry
 
     manifest.to_code = to_code_testing
diff --git a/tests/unit_tests/core/test_config.py b/tests/unit_tests/core/test_config.py
index 07cff003cd..0db7039668 100644
--- a/tests/unit_tests/core/test_config.py
+++ b/tests/unit_tests/core/test_config.py
@@ -9,6 +9,7 @@ from unittest.mock import MagicMock, Mock, patch
 import pytest
 
 from esphome import config_validation as cv, core
+import esphome.codegen as cg
 from esphome.components.safe_mode import to_code as safe_mode_to_code
 from esphome.const import (
     CONF_AREA,
@@ -23,7 +24,7 @@ from esphome.const import (
     KEY_TARGET_PLATFORM,
     Toolchain,
 )
-from esphome.core import CORE, config
+from esphome.core import CORE, KEY_CONTROLLER_REGISTRY_CONTROLLERS, config
 from esphome.core.config import (
     Area,
     make_app_name_cpp,
@@ -455,6 +456,35 @@ async def test_add_looping_components_with_entries() -> None:
     assert "(1 * HasLoopOverride<esphome::logger::Logger>::value)" in text
 
 
+@pytest.mark.asyncio
+async def test_add_controller_registry_dispatch_without_controllers() -> None:
+    """Nothing is emitted when no controller registered."""
+    CORE.data.pop(KEY_CONTROLLER_REGISTRY_CONTROLLERS, None)
+
+    await config._add_controller_registry_dispatch()
+
+    assert "USE_CONTROLLER_REGISTRY" not in {d.name for d in CORE.defines}
+    assert not [s for s in CORE.global_statements if "controller" in str(s)]
+
+
+@pytest.mark.asyncio
+async def test_add_controller_registry_dispatch_with_controllers() -> None:
+    """Registered controllers become one tuple plus the dispatch include."""
+    CORE.register_controller(cg.MockObj("api_apiserver_id"))
+    CORE.register_controller(cg.MockObj("web_server_webserver_id"))
+
+    await config._add_controller_registry_dispatch()
+
+    assert "USE_CONTROLLER_REGISTRY" in {d.name for d in CORE.defines}
+    statements = [str(s) for s in CORE.global_statements]
+    assert "#include <tuple>" in statements
+    assert (
+        "static auto esphome_controllers() { return std::tuple{api_apiserver_id, web_server_webserver_id}; }"
+        in statements
+    )
+    assert '#include "esphome/core/controller_dispatch.h"' in statements
+
+
 def test_valid_include_with_angle_brackets() -> None:
     """Test valid_include accepts angle bracket includes."""
     assert valid_include("<ArduinoJson.h>") == "<ArduinoJson.h>"
diff --git a/tests/unit_tests/test_codegen.py b/tests/unit_tests/test_codegen.py
index 8d01fef7c2..c5c971b22d 100644
--- a/tests/unit_tests/test_codegen.py
+++ b/tests/unit_tests/test_codegen.py
@@ -70,7 +70,6 @@ from esphome.cpp_generator import _extract_component_ns
         "arduino_json_ns",
         "JsonObject",
         "JsonObjectConst",
-        "Controller",
         "GPIOPin",
     ),
 )