diff --git a/esphome/components/esphome/ota/__init__.py b/esphome/components/esphome/ota/__init__.py
index 337064dd271..d3584380961 100644
--- a/esphome/components/esphome/ota/__init__.py
+++ b/esphome/components/esphome/ota/__init__.py
@@ -78,6 +78,20 @@ def ota_esphome_final_validate(config):
         else:
             new_ota_conf.append(ota_conf)
 
+    # BREAKING CHANGE: Only a single ESPHome OTA instance is supported. Historically
+    # the config layer merged multiple configs by port to accommodate users who had a
+    # local 'ota:' block and then imported a remote package that also declared one —
+    # the merge kept their build working. That merge behavior is preserved. But two
+    # ESPHome OTA instances on *different* ports is not a real-world use case and
+    # creates ambiguity for listeners, socket wake hooks, and safe_mode coordination.
+    if len(merged_ota_esphome_configs_by_port) > 1:
+        raise cv.Invalid(
+            f"Only a single '{CONF_OTA}' '{CONF_PLATFORM}: {CONF_ESPHOME}' instance is "
+            f"supported, but multiple were configured on different ports "
+            f"({sorted(merged_ota_esphome_configs_by_port.keys())}). Remove the extra "
+            f"configurations or place them on the same port so they can be merged."
+        )
+
     new_ota_conf.extend(merged_ota_esphome_configs_by_port.values())
 
     full_conf[CONF_OTA] = new_ota_conf
diff --git a/esphome/core/application.h b/esphome/core/application.h
index 63a951b6814..100ff3440dc 100644
--- a/esphome/core/application.h
+++ b/esphome/core/application.h
@@ -564,11 +564,16 @@ class Application {
   /// a new connection arrives on the listening socket. OTA disables its own
   /// loop while idle to avoid per-tick dispatch overhead.
   void set_ota_wake_component(Component *component) { this->ota_wake_component_ = component; }
-  /// Wake the registered OTA component (if any) from any context. Safe to call
-  /// from the LwIP TCP/IP task and other callback contexts.
+  /// Mark the registered OTA component (if any) for loop re-enable from any
+  /// context. Intentionally does NOT call wake_loop_any_context() — every
+  /// caller (lwip fast-select callback, raw-tcp accept callback, host
+  /// select() return path) has already woken the main loop, so a second wake
+  /// here would be redundant. Application is a friend of Component, so we
+  /// set the pending-enable flags directly.
   void IRAM_ATTR wake_ota_component_any_context() {
     if (this->ota_wake_component_ != nullptr) {
-      this->ota_wake_component_->enable_loop_soon_any_context();
+      this->ota_wake_component_->pending_enable_loop_ = true;
+      this->has_pending_enable_loop_requests_ = true;
     }
   }
 #endif