diff --git a/esphome/components/ota/ota_backend.cpp b/esphome/components/ota/ota_backend.cpp
index 0447b968a3..a83195d42d 100644
--- a/esphome/components/ota/ota_backend.cpp
+++ b/esphome/components/ota/ota_backend.cpp
@@ -1,5 +1,9 @@
 #include "ota_backend.h"
 
+#ifdef ESPHOME_THREAD_MULTI_ATOMICS
+#include <atomic>
+#endif
+
 namespace esphome::ota {
 
 bool version_is_older(const char *candidate, const char *reference) {
@@ -30,6 +34,60 @@ bool version_is_older(const char *candidate, const char *reference) {
   }
 }
 
+// Non-blocking; may be released by another task than the one that took it.
+#ifdef ESPHOME_THREAD_MULTI_ATOMICS
+// uint32_t: narrower atomics compile to a masked CAS on Xtensa.
+static std::atomic<uint32_t> update_locked{0};  // NOLINT(cppcoreguidelines-avoid-non-const-global-variables)
+
+static bool update_lock_test_and_set() { return update_locked.exchange(1) == 0; }
+static void update_lock_clear() { update_locked.store(0); }
+#else
+static bool update_locked = false;  // NOLINT(cppcoreguidelines-avoid-non-const-global-variables)
+
+#ifdef ESPHOME_THREAD_MULTI_NO_ATOMICS
+// BK72xx has no atomic exchange.
+static Mutex &update_lock_mutex() {
+  static Mutex mutex;
+  return mutex;
+}
+#endif
+
+static bool update_lock_test_and_set() {
+#ifdef ESPHOME_THREAD_MULTI_NO_ATOMICS
+  LockGuard guard(update_lock_mutex());
+#else
+  // lwIP callbacks may run from an interrupt (RP2040).
+  InterruptLock guard;
+#endif
+  if (update_locked)
+    return false;
+  update_locked = true;
+  return true;
+}
+
+static void update_lock_clear() {
+#ifdef ESPHOME_THREAD_MULTI_NO_ATOMICS
+  LockGuard guard(update_lock_mutex());
+#endif
+  update_locked = false;
+}
+#endif
+
+bool UpdateLock::try_acquire() {
+  if (!this->held_)
+    this->held_ = update_lock_test_and_set();
+  return this->held_;
+}
+
+void UpdateLock::release() {
+  if (!this->held_)
+    return;
+  update_lock_clear();
+  this->held_ = false;
+}
+
+void UpdateLock::force_release() { update_lock_clear(); }
+
 #ifdef USE_OTA_STATE_LISTENER
 OTAGlobalCallback *global_ota_callback{nullptr};  // NOLINT(cppcoreguidelines-avoid-non-const-global-variables)
 
diff --git a/esphome/components/ota/ota_backend.h b/esphome/components/ota/ota_backend.h
index a505d58efe..840d1ac11c 100644
--- a/esphome/components/ota/ota_backend.h
+++ b/esphome/components/ota/ota_backend.h
@@ -51,6 +51,7 @@ enum OTAResponseTypes {
   OTA_RESPONSE_ERROR_BOOTLOADER_UPDATE = 0x92,
   OTA_RESPONSE_ERROR_VERSION_DOWNGRADE = 0x93,
   OTA_RESPONSE_ERROR_ENCRYPTION_REQUIRED = 0x94,
+  OTA_RESPONSE_ERROR_UPDATE_BUSY = 0x95,
   OTA_RESPONSE_ERROR_UNKNOWN = 0xFF,
 };
 
@@ -95,6 +96,29 @@ enum OTAType : uint8_t {
   OTA_TYPE_UPDATE_BOOTLOADER = 0x02,
 };
 
+/// Serializes flash updates. Taken in begin(), released when the backend is destroyed, or kept until
+/// reboot after a successful end(). Also for components writing the update partition outside OTA.
+class UpdateLock {
+ public:
+  UpdateLock() = default;
+  ~UpdateLock() { this->release(); }
+  UpdateLock(const UpdateLock &) = delete;
+  UpdateLock &operator=(const UpdateLock &) = delete;
+
+  /// Returns false if held elsewhere.
+  bool try_acquire();
+  void release();
+  bool is_held() const { return this->held_; }
+  /// Keep the lock set until reboot; is_held() becomes false.
+  void hold_until_reboot() { this->held_ = false; }
+
+ protected:
+  /// Tests only.
+  static void force_release();
+
+  bool held_{false};
+};
+
 // The OTA backend method surface. Exactly one backend exists per build,
 // selected in ota_backend_factory.h where this concept is asserted on
 // make_ota_backend()'s return type. Semantics beyond the signatures:
diff --git a/esphome/components/ota/ota_backend_arduino_libretiny.cpp b/esphome/components/ota/ota_backend_arduino_libretiny.cpp
index 02a5c5750f..33af42b6a7 100644
--- a/esphome/components/ota/ota_backend_arduino_libretiny.cpp
+++ b/esphome/components/ota/ota_backend_arduino_libretiny.cpp
@@ -14,6 +14,8 @@ ESPHOME_LOG_TAG(TAG, "ota");
 std::unique_ptr<ArduinoLibreTinyOTABackend> make_ota_backend() { return make_unique<ArduinoLibreTinyOTABackend>(); }
 
 OTAResponseTypes ArduinoLibreTinyOTABackend::begin(size_t image_size, OTAType ota_type) {
+  if (!this->lock_.try_acquire())
+    return OTA_RESPONSE_ERROR_UPDATE_BUSY;
   if (ota_type != OTA_TYPE_UPDATE_APP) {
     return OTA_RESPONSE_ERROR_UNSUPPORTED_OTA_TYPE;
   }
@@ -57,6 +59,7 @@ OTAResponseTypes ArduinoLibreTinyOTABackend::end() {
   // Use strict validation (false) when MD5 is set, lenient validation (true) when no MD5
   // This matches the behavior of the old web_server OTA implementation
   if (Update.end(!this->md5_set_)) {
+    this->lock_.hold_until_reboot();
     return OTA_RESPONSE_OK;
   }
 
@@ -66,7 +69,11 @@ OTAResponseTypes ArduinoLibreTinyOTABackend::end() {
   return OTA_RESPONSE_ERROR_UPDATE_END;
 }
 
-void ArduinoLibreTinyOTABackend::abort() { Update.abort(); }
+void ArduinoLibreTinyOTABackend::abort() {
+  if (!this->lock_.is_held())  // refused in begin()
+    return;
+  Update.abort();
+}
 
 }  // namespace esphome::ota
 #endif  // USE_LIBRETINY
diff --git a/esphome/components/ota/ota_backend_arduino_libretiny.h b/esphome/components/ota/ota_backend_arduino_libretiny.h
index c322ed21f2..fc277bb5e4 100644
--- a/esphome/components/ota/ota_backend_arduino_libretiny.h
+++ b/esphome/components/ota/ota_backend_arduino_libretiny.h
@@ -16,6 +16,7 @@ class ArduinoLibreTinyOTABackend final {
   static constexpr bool supports_compression() { return false; }
 
  private:
+  UpdateLock lock_;
   bool md5_set_{false};
 };
 
diff --git a/esphome/components/ota/ota_backend_arduino_rp2.cpp b/esphome/components/ota/ota_backend_arduino_rp2.cpp
index 74f44c0b3b..d4d94be236 100644
--- a/esphome/components/ota/ota_backend_arduino_rp2.cpp
+++ b/esphome/components/ota/ota_backend_arduino_rp2.cpp
@@ -16,6 +16,8 @@ ESPHOME_LOG_TAG(TAG, "ota");
 std::unique_ptr<ArduinoRP2OTABackend> make_ota_backend() { return make_unique<ArduinoRP2OTABackend>(); }
 
 OTAResponseTypes ArduinoRP2OTABackend::begin(size_t image_size, OTAType ota_type) {
+  if (!this->lock_.try_acquire())
+    return OTA_RESPONSE_ERROR_UPDATE_BUSY;
   if (ota_type != OTA_TYPE_UPDATE_APP) {
     return OTA_RESPONSE_ERROR_UNSUPPORTED_OTA_TYPE;
   }
@@ -63,6 +65,7 @@ OTAResponseTypes ArduinoRP2OTABackend::end() {
   // Use strict validation (false) when MD5 is set, lenient validation (true) when no MD5
   // This matches the behavior of the old web_server OTA implementation
   if (Update.end(!this->md5_set_)) {
+    this->lock_.hold_until_reboot();
     return OTA_RESPONSE_OK;
   }
 
@@ -73,6 +76,8 @@ OTAResponseTypes ArduinoRP2OTABackend::end() {
 }
 
 void ArduinoRP2OTABackend::abort() {
+  if (!this->lock_.is_held())  // refused in begin()
+    return;
   Update.end();
   rp2::preferences_prevent_write(false);
 }
diff --git a/esphome/components/ota/ota_backend_arduino_rp2.h b/esphome/components/ota/ota_backend_arduino_rp2.h
index 15142869ac..93b9dcb75c 100644
--- a/esphome/components/ota/ota_backend_arduino_rp2.h
+++ b/esphome/components/ota/ota_backend_arduino_rp2.h
@@ -21,6 +21,7 @@ class ArduinoRP2OTABackend final {
   static constexpr bool supports_compression() { return USE_ARDUINO_VERSION_CODE >= VERSION_CODE(4, 0, 3); }
 
  private:
+  UpdateLock lock_;
   bool md5_set_{false};
 };
 
diff --git a/esphome/components/ota/ota_backend_esp8266.cpp b/esphome/components/ota/ota_backend_esp8266.cpp
index 5be55a5200..3d6148e64f 100644
--- a/esphome/components/ota/ota_backend_esp8266.cpp
+++ b/esphome/components/ota/ota_backend_esp8266.cpp
@@ -51,6 +51,8 @@ ESPHOME_LOG_TAG(TAG, "ota");
 std::unique_ptr<ESP8266OTABackend> make_ota_backend() { return make_unique<ESP8266OTABackend>(); }
 
 OTAResponseTypes ESP8266OTABackend::begin(size_t image_size, OTAType ota_type) {
+  if (!this->lock_.try_acquire())
+    return OTA_RESPONSE_ERROR_UPDATE_BUSY;
   if (ota_type != OTA_TYPE_UPDATE_APP) {
     return OTA_RESPONSE_ERROR_UNSUPPORTED_OTA_TYPE;
   }
@@ -303,10 +305,13 @@ OTAResponseTypes ESP8266OTABackend::end() {
   this->buffer_.reset();
   esp8266::preferences_prevent_write(false);
 
+  this->lock_.hold_until_reboot();
   return OTA_RESPONSE_OK;
 }
 
 void ESP8266OTABackend::abort() {
+  if (!this->lock_.is_held())  // refused in begin()
+    return;
   this->buffer_.reset();
   this->buffer_len_ = 0;
   this->image_size_ = 0;
diff --git a/esphome/components/ota/ota_backend_esp8266.h b/esphome/components/ota/ota_backend_esp8266.h
index 1f1ec37eee..bd4c9a1bce 100644
--- a/esphome/components/ota/ota_backend_esp8266.h
+++ b/esphome/components/ota/ota_backend_esp8266.h
@@ -23,6 +23,7 @@ class ESP8266OTABackend final {
   static constexpr bool supports_compression() { return true; }
 
  protected:
+  UpdateLock lock_;
   /// Erase flash sector if current address is at sector boundary
   bool erase_sector_if_needed_();
 
diff --git a/esphome/components/ota/ota_backend_esp_idf.cpp b/esphome/components/ota/ota_backend_esp_idf.cpp
index 2316aad5cf..fd6fd7f6f1 100644
--- a/esphome/components/ota/ota_backend_esp_idf.cpp
+++ b/esphome/components/ota/ota_backend_esp_idf.cpp
@@ -20,6 +20,8 @@ ESPHOME_LOG_TAG(TAG, "ota");
 std::unique_ptr<IDFOTABackend> make_ota_backend() { return make_unique<IDFOTABackend>(); }
 
 OTAResponseTypes IDFOTABackend::begin(size_t image_size, ota::OTAType ota_type) {
+  if (!this->lock_.try_acquire())
+    return OTA_RESPONSE_ERROR_UPDATE_BUSY;
 #ifdef USE_OTA_PARTITIONS
   this->ota_type_ = ota_type;
   if (this->ota_type_ == ota::OTA_TYPE_UPDATE_PARTITION_TABLE) {
@@ -196,7 +198,7 @@ OTAResponseTypes IDFOTABackend::end() {
   // signature, and only re-points boot at an already-installed app -- so it is
   // intentionally not run through the signature verifier below.
   if (this->ota_type_ == ota::OTA_TYPE_UPDATE_PARTITION_TABLE) {
-    return this->update_partition_table();
+    return this->hold_lock_if_ok_(this->update_partition_table());
   }
   if (!this->is_app_or_bootloader_update_()) {
     return OTA_RESPONSE_ERROR_UNSUPPORTED_OTA_TYPE;
@@ -209,7 +211,7 @@ OTAResponseTypes IDFOTABackend::end() {
   }
 #ifdef USE_OTA_PARTITIONS
   if (this->ota_type_ == ota::OTA_TYPE_UPDATE_BOOTLOADER) {
-    return this->finalize_bootloader_update_(err);
+    return this->hold_lock_if_ok_(this->finalize_bootloader_update_(err));
   }
 #endif
   if (err == ESP_OK) {
@@ -242,7 +244,7 @@ OTAResponseTypes IDFOTABackend::end() {
 #endif
     err = esp_ota_set_boot_partition(this->partition_);
     if (err == ESP_OK) {
-      return OTA_RESPONSE_OK;
+      return this->hold_lock_if_ok_(OTA_RESPONSE_OK);
     }
   }
   if (err == ESP_ERR_OTA_VALIDATE_FAILED) {
@@ -260,6 +262,8 @@ OTAResponseTypes IDFOTABackend::end() {
 }
 
 void IDFOTABackend::abort() {
+  if (!this->lock_.is_held())  // refused in begin()
+    return;
 #ifdef USE_OTA_PARTITIONS
   if (this->partition_table_part_ != nullptr) {
     esp_partition_deregister_external(this->partition_table_part_);
diff --git a/esphome/components/ota/ota_backend_esp_idf.h b/esphome/components/ota/ota_backend_esp_idf.h
index 4f4093a594..d166bb361f 100644
--- a/esphome/components/ota/ota_backend_esp_idf.h
+++ b/esphome/components/ota/ota_backend_esp_idf.h
@@ -36,6 +36,12 @@ class IDFOTABackend final {
   static constexpr bool supports_compression() { return false; }
 
  protected:
+  UpdateLock lock_;
+  OTAResponseTypes hold_lock_if_ok_(OTAResponseTypes result) {
+    if (result == OTA_RESPONSE_OK)
+      this->lock_.hold_until_reboot();
+    return result;
+  }
 #ifdef USE_OTA_PARTITIONS
   // copy_dest_part non-null means the running app must be copied INTO this slot of the current
   // table before the new partition table is committed. The destination is in the current table
diff --git a/esphome/components/ota/ota_backend_host.cpp b/esphome/components/ota/ota_backend_host.cpp
index 456fbb5863..923b0afe18 100644
--- a/esphome/components/ota/ota_backend_host.cpp
+++ b/esphome/components/ota/ota_backend_host.cpp
@@ -200,6 +200,8 @@ bool validate_executable_(const char *staging_path, const std::string &exe_path)
 std::unique_ptr<HostOTABackend> make_ota_backend() { return make_unique<HostOTABackend>(); }
 
 OTAResponseTypes HostOTABackend::begin(size_t image_size, OTAType ota_type) {
+  if (!this->lock_.try_acquire())
+    return OTA_RESPONSE_ERROR_UPDATE_BUSY;
   if (ota_type != OTA_TYPE_UPDATE_APP)
     return OTA_RESPONSE_ERROR_UNSUPPORTED_OTA_TYPE;
   // 0 = unknown size (web_server multipart); cap at MAX_OTA_SIZE.
@@ -318,10 +320,13 @@ OTAResponseTypes HostOTABackend::end() {
   host::arm_reexec(this->final_path_);
   this->staging_path_.clear();
   ESP_LOGI(TAG, "OTA staged at %s; will re-exec on reboot", this->final_path_.c_str());
+  this->lock_.hold_until_reboot();
   return OTA_RESPONSE_OK;
 }
 
 void HostOTABackend::abort() {
+  if (!this->lock_.is_held())  // refused in begin()
+    return;
   if (this->fd_ >= 0) {
     ::close(this->fd_);
     this->fd_ = -1;
diff --git a/esphome/components/ota/ota_backend_host.h b/esphome/components/ota/ota_backend_host.h
index e53868f102..6c86fe10ba 100644
--- a/esphome/components/ota/ota_backend_host.h
+++ b/esphome/components/ota/ota_backend_host.h
@@ -22,6 +22,7 @@ class HostOTABackend final {
   static constexpr bool supports_compression() { return false; }
 
  protected:
+  UpdateLock lock_;
   md5::MD5Digest md5_{};
   std::string staging_path_;
   std::string final_path_;
diff --git a/esphome/components/web_server/ota/ota_web_server.cpp b/esphome/components/web_server/ota/ota_web_server.cpp
index 3cf1d9802e..8a668ae0fc 100644
--- a/esphome/components/web_server/ota/ota_web_server.cpp
+++ b/esphome/components/web_server/ota/ota_web_server.cpp
@@ -9,12 +9,6 @@
 #include "esphome/components/captive_portal/captive_portal.h"
 #endif
 
-#ifdef USE_ARDUINO
-#if defined(USE_LIBRETINY)
-#include <Update.h>
-#endif
-#endif  // USE_ARDUINO
-
 #if USE_ESP32
 using PlatformString = std::string;
 #elif USE_ARDUINO
@@ -64,6 +58,10 @@ class OTARequestHandler : public AsyncWebHandler {
   void report_ota_progress_(AsyncWebServerRequest *request);
   void schedule_ota_reboot_();
   void ota_init_(const char *filename);
+  /// Abort and drop the backend, releasing the lock.
+  void abort_session_();
+  /// Reply "busy" without touching the running upload.
+  void refuse_(AsyncWebServerRequest *request);
 
   uint32_t last_ota_progress_{0};
   uint32_t ota_read_length_{0};
@@ -72,6 +70,9 @@ class OTARequestHandler : public AsyncWebHandler {
 
  private:
   ota::OTABackendPtr ota_backend_{nullptr};
+  /// Request that owns ota_backend_.
+  const AsyncWebServerRequest *ota_request_{nullptr};
+  const AsyncWebServerRequest *refused_request_{nullptr};
 };
 
 void OTARequestHandler::report_ota_progress_(AsyncWebServerRequest *request) {
@@ -118,38 +119,13 @@ void OTARequestHandler::handleUpload(AsyncWebServerRequest *request, const Platf
   // fires a separate start-marker call with data==nullptr/len==0 before the
   // first real chunk; gate on len>0 so we only trigger once per upload.)
   if (index == 0 && len > 0) {
-    // If a previous upload was interrupted (e.g. client closed the tab, TCP
-    // reset) the backend from that session may still be open. Tear it down
-    // so flash state doesn't get concatenated with the new image (which can
-    // produce a technically-valid-sized but corrupted firmware that bricks
-    // the device once it reboots).
+    // A stalled upload times out and onDisconnect() frees it, so refusing can't block for long.
     if (this->ota_backend_) {
-      ESP_LOGW(TAG, "New OTA upload received while previous session was still open; aborting previous session");
-      this->ota_backend_->abort();
-#ifdef USE_OTA_STATE_LISTENER
-      // Notify listeners that the previous session was aborted before the new one starts.
-      this->parent_->notify_state_deferred_(ota::OTA_ABORT, 0.0f, 0);
-#endif
-      this->ota_backend_.reset();
+      ESP_LOGW(TAG, "OTA upload refused: another upload is in progress");
+      this->refuse_(request);
+      return;
     }
 
-    // Initialize OTA on first call
-    this->ota_init_(filename.c_str());
-
-#ifdef USE_OTA_STATE_LISTENER
-    // Notify OTA started - use notify_state_deferred_ since we're in web server task
-    this->parent_->notify_state_deferred_(ota::OTA_STARTED, 0.0f, 0);
-#endif
-
-    // Platform-specific pre-initialization
-#ifdef USE_ARDUINO
-#if defined(USE_LIBRETINY)
-    if (Update.isRunning()) {
-      Update.abort();
-    }
-#endif
-#endif  // USE_ARDUINO
-
     this->ota_backend_ = ota::make_ota_backend();
     if (!this->ota_backend_) {
       ESP_LOGE(TAG, "Failed to create OTA backend");
@@ -164,6 +140,22 @@ void OTARequestHandler::handleUpload(AsyncWebServerRequest *request, const Platf
     // is unknown (contentLength includes multipart overhead)
     // Pass 0 to indicate unknown size
     error_code = this->ota_backend_->begin(0);
+    if (error_code == ota::OTA_RESPONSE_ERROR_UPDATE_BUSY) {
+      // Nothing started: no state notifications.
+      ESP_LOGW(TAG, "OTA upload refused: another update is in progress");
+      this->ota_backend_.reset();
+      this->refuse_(request);
+      return;
+    }
+
+    // Initialize OTA on first call
+    this->ota_init_(filename.c_str());
+
+#ifdef USE_OTA_STATE_LISTENER
+    // Notify OTA started - use notify_state_deferred_ since we're in web server task
+    this->parent_->notify_state_deferred_(ota::OTA_STARTED, 0.0f, 0);
+#endif
+
     if (error_code != ota::OTA_RESPONSE_OK) {
       ESP_LOGE(TAG, "OTA begin failed: %d", error_code);
       this->ota_backend_.reset();
@@ -172,9 +164,18 @@ void OTARequestHandler::handleUpload(AsyncWebServerRequest *request, const Platf
 #endif
       return;
     }
+
+    // An interrupted upload gets no final chunk.
+    this->ota_request_ = request;
+    request->onDisconnect([this, request]() {
+      if (this->ota_request_ == request && this->ota_backend_) {
+        ESP_LOGW(TAG, "OTA upload interrupted; aborting");
+        this->abort_session_();
+      }
+    });
   }
 
-  if (!this->ota_backend_) {
+  if (!this->ota_backend_ || request != this->ota_request_) {
     return;
   }
 
@@ -185,6 +186,7 @@ void OTARequestHandler::handleUpload(AsyncWebServerRequest *request, const Platf
       ESP_LOGE(TAG, "OTA write failed: %d", error_code);
       this->ota_backend_->abort();
       this->ota_backend_.reset();
+      this->ota_request_ = nullptr;
 #ifdef USE_OTA_STATE_LISTENER
       this->parent_->notify_state_deferred_(ota::OTA_ERROR, 0.0f, static_cast<uint8_t>(error_code));
 #endif
@@ -212,28 +214,54 @@ void OTARequestHandler::handleUpload(AsyncWebServerRequest *request, const Platf
       this->schedule_ota_reboot_();
     } else {
       ESP_LOGE(TAG, "OTA end failed: %d", error_code);
+      // Reset the platform updater before the lock is released.
+      this->ota_backend_->abort();
 #ifdef USE_OTA_STATE_LISTENER
       this->parent_->notify_state_deferred_(ota::OTA_ERROR, 0.0f, static_cast<uint8_t>(error_code));
 #endif
     }
     this->ota_backend_.reset();
+    this->ota_request_ = nullptr;
   }
 }
 
+void OTARequestHandler::abort_session_() {
+  this->ota_backend_->abort();
+#ifdef USE_OTA_STATE_LISTENER
+  this->parent_->notify_state_deferred_(ota::OTA_ABORT, 0.0f, 0);
+#endif
+  this->ota_backend_.reset();
+  this->ota_request_ = nullptr;
+}
+
+void OTARequestHandler::refuse_(AsyncWebServerRequest *request) {
+  this->refused_request_ = request;
+  request->onDisconnect([this, request]() {
+    if (this->refused_request_ == request)
+      this->refused_request_ = nullptr;
+  });
+}
+
 void OTARequestHandler::handleRequest(AsyncWebServerRequest *request) {
   AsyncWebServerResponse *response;
   // Use the ota_success_ flag to determine the actual result
+  const bool refused = request == this->refused_request_;
+  if (refused)
+    this->refused_request_ = nullptr;
 #ifdef USE_ESP8266
   static const char UPDATE_SUCCESS[] PROGMEM = "Update Successful!";
   static const char UPDATE_FAILED[] PROGMEM = "Update Failed!";
+  static const char UPDATE_BUSY[] PROGMEM = "Update Failed! Another update is in progress, retry later.";
   static const char TEXT_PLAIN[] PROGMEM = "text/plain";
   static const char CONNECTION_STR[] PROGMEM = "Connection";
   static const char CLOSE_STR[] PROGMEM = "close";
-  const char *msg = this->ota_success_ ? UPDATE_SUCCESS : UPDATE_FAILED;
+  const char *msg = refused ? UPDATE_BUSY : (this->ota_success_ ? UPDATE_SUCCESS : UPDATE_FAILED);
   response = request->beginResponse_P(200, TEXT_PLAIN, msg);
   response->addHeader(CONNECTION_STR, CLOSE_STR);
 #else
-  const char *msg = this->ota_success_ ? "Update Successful!" : "Update Failed!";
+  const char *msg = refused              ? "Update Failed! Another update is in progress, retry later."
+                    : this->ota_success_ ? "Update Successful!"
+                                         : "Update Failed!";
   response = request->beginResponse(200, "text/plain", msg);
   response->addHeader("Connection", "close");
 #endif
diff --git a/esphome/components/web_server_idf/web_server_idf.cpp b/esphome/components/web_server_idf/web_server_idf.cpp
index 2153e232a0..d9a7d65e8c 100644
--- a/esphome/components/web_server_idf/web_server_idf.cpp
+++ b/esphome/components/web_server_idf/web_server_idf.cpp
@@ -311,6 +311,10 @@ esp_err_t AsyncWebServer::handle_raw_body_(httpd_req_t *r, const char *content_t
 }
 
 AsyncWebServerRequest::~AsyncWebServerRequest() {
+#ifdef USE_WEBSERVER_OTA
+  if (this->on_disconnect_)
+    this->on_disconnect_();
+#endif
   delete this->rsp_;
   for (auto *param : this->params_) {
     delete param;  // NOLINT(cppcoreguidelines-owning-memory)
diff --git a/esphome/components/web_server_idf/web_server_idf.h b/esphome/components/web_server_idf/web_server_idf.h
index f9094b05c5..4d4490d907 100644
--- a/esphome/components/web_server_idf/web_server_idf.h
+++ b/esphome/components/web_server_idf/web_server_idf.h
@@ -183,6 +183,12 @@ class AsyncWebServerRequest {
   std::string arg(const char *name);
   std::string arg(const std::string &name) { return this->arg(name.c_str()); }
 
+#ifdef USE_WEBSERVER_OTA
+  /// Called when the request ends, including early returns.
+  // NOLINTNEXTLINE(readability-identifier-naming)
+  void onDisconnect(std::function<void()> fn) { this->on_disconnect_ = std::move(fn); }
+#endif
+
   operator httpd_req_t *() const { return this->req_; }
   optional<std::string> get_header(const char *name) const;
   // NOLINTNEXTLINE(readability-identifier-naming)
@@ -198,6 +204,9 @@ class AsyncWebServerRequest {
   optional<std::string> find_query_value_(const char *name) const;
   std::vector<AsyncWebParameter *> params_;
   std::string post_query_;
+#ifdef USE_WEBSERVER_OTA
+  std::function<void()> on_disconnect_;
+#endif
   AsyncWebServerRequest(httpd_req_t *req) : req_(req) {}
   AsyncWebServerRequest(httpd_req_t *req, std::string post_query) : req_(req), post_query_(std::move(post_query)) {}
   void init_response_(AsyncWebServerResponse *rsp, int code, const char *content_type);
diff --git a/esphome/espota2.py b/esphome/espota2.py
index f775afe7f6..d8a2ff9000 100644
--- a/esphome/espota2.py
+++ b/esphome/espota2.py
@@ -54,6 +54,7 @@ RESPONSE_ERROR_BOOTLOADER_VERIFY = 0x91
 RESPONSE_ERROR_BOOTLOADER_UPDATE = 0x92
 RESPONSE_ERROR_VERSION_DOWNGRADE = 0x93
 RESPONSE_ERROR_ENCRYPTION_REQUIRED = 0x94
+RESPONSE_ERROR_UPDATE_BUSY = 0x95
 RESPONSE_ERROR_UNKNOWN = 0xFF
 
 OTA_VERSION_1_0 = 1
@@ -203,6 +204,10 @@ _ERROR_MESSAGES: dict[int, str] = {
         "of the YAML this upload uses, or update your esphome installation if it "
         "predates OTA encryption."
     ),
+    RESPONSE_ERROR_UPDATE_BUSY: (
+        "The device is busy with another update that writes to its flash. "
+        "Wait for it to finish, then retry."
+    ),
     RESPONSE_ERROR_UNKNOWN: "Unknown error from ESP",
 }
 
diff --git a/tests/components/ota/test_update_lock.cpp b/tests/components/ota/test_update_lock.cpp
new file mode 100644
index 0000000000..28314cb1c2
--- /dev/null
+++ b/tests/components/ota/test_update_lock.cpp
@@ -0,0 +1,85 @@
+#include <gtest/gtest.h>
+
+#include "esphome/components/ota/ota_backend_factory.h"
+
+namespace esphome::ota::testing {
+
+TEST(UpdateLock, SecondHolderIsRefused) {
+  UpdateLock first;
+  UpdateLock second;
+  EXPECT_TRUE(first.try_acquire());
+  EXPECT_FALSE(second.try_acquire());
+  first.release();
+  EXPECT_TRUE(second.try_acquire());
+}
+
+TEST(UpdateLock, AcquireIsIdempotentForTheHolder) {
+  UpdateLock lock;
+  EXPECT_TRUE(lock.try_acquire());
+  EXPECT_TRUE(lock.try_acquire());
+  lock.release();
+  UpdateLock other;
+  EXPECT_TRUE(other.try_acquire());
+}
+
+TEST(UpdateLock, ReleaseByNonHolderKeepsLock) {
+  UpdateLock holder;
+  UpdateLock other;
+  EXPECT_TRUE(holder.try_acquire());
+  other.release();
+  EXPECT_FALSE(other.try_acquire());
+}
+
+TEST(UpdateLock, DestructorReleases) {
+  {
+    UpdateLock scoped;
+    EXPECT_TRUE(scoped.try_acquire());
+  }
+  UpdateLock next;
+  EXPECT_TRUE(next.try_acquire());
+}
+
+TEST(UpdateLock, IsHeldTracksOwnership) {
+  UpdateLock holder;
+  UpdateLock other;
+  EXPECT_FALSE(holder.is_held());
+  EXPECT_TRUE(holder.try_acquire());
+  EXPECT_TRUE(holder.is_held());
+  EXPECT_FALSE(other.try_acquire());
+  EXPECT_FALSE(other.is_held());
+}
+
+class TestUpdateLock : public UpdateLock {
+ public:
+  using UpdateLock::force_release;
+};
+
+TEST(UpdateLock, HoldUntilRebootOutlivesHolder) {
+  {
+    UpdateLock committed;
+    EXPECT_TRUE(committed.try_acquire());
+    committed.hold_until_reboot();
+    EXPECT_FALSE(committed.is_held());
+  }
+  UpdateLock next;
+  EXPECT_FALSE(next.try_acquire());
+  TestUpdateLock::force_release();
+  EXPECT_TRUE(next.try_acquire());
+}
+
+TEST(UpdateLock, SecondBackendBeginIsBusy) {
+  auto first = make_ota_backend();
+  auto second = make_ota_backend();
+  ASSERT_EQ(first->begin(1024), OTA_RESPONSE_OK);
+  EXPECT_EQ(second->begin(1024), OTA_RESPONSE_ERROR_UPDATE_BUSY);
+  // Native OTA calls abort() after a refused begin().
+  second->abort();
+  uint8_t data[16] = {};
+  EXPECT_EQ(first->write(data, sizeof(data)), OTA_RESPONSE_OK);
+  first->abort();
+  first.reset();
+  EXPECT_EQ(second->begin(1024), OTA_RESPONSE_OK);
+  second->abort();
+}
+
+}  // namespace esphome::ota::testing
diff --git a/tests/unit_tests/test_espota2.py b/tests/unit_tests/test_espota2.py
index 6fa6c616b6..f1e04da8c8 100644
--- a/tests/unit_tests/test_espota2.py
+++ b/tests/unit_tests/test_espota2.py
@@ -263,6 +263,7 @@ def test_receive_exactly_closed_connection_is_network_error(mock_socket: Mock) -
             espota2.RESPONSE_ERROR_BOOTLOADER_UPDATE,
             "An error occurred while updating the bootloader",
         ),
+        (espota2.RESPONSE_ERROR_UPDATE_BUSY, "The device is busy with another update"),
         (espota2.RESPONSE_ERROR_UNKNOWN, "Unknown error from ESP"),
     ],
 )