diff --git a/esphome/components/web_server/ota/ota_web_server.cpp b/esphome/components/web_server/ota/ota_web_server.cpp
index 9812714ec03..95763e2daf0 100644
--- a/esphome/components/web_server/ota/ota_web_server.cpp
+++ b/esphome/components/web_server/ota/ota_web_server.cpp
@@ -249,7 +249,7 @@ void WebServerOTAComponent::setup() {
     return;
   }
 
-  // AsyncWebServer takes ownership of the handler and will delete it when the server is destroyed
+  // The handler lives for the life of the process; WebServerBase never destroys its server
   base->add_handler(new OTARequestHandler(this));  // NOLINT
 }
 
diff --git a/esphome/components/web_server_base/web_server_base.h b/esphome/components/web_server_base/web_server_base.h
index c647a13b50b..94579de70f8 100644
--- a/esphome/components/web_server_base/web_server_base.h
+++ b/esphome/components/web_server_base/web_server_base.h
@@ -112,9 +112,18 @@ class AuthMiddlewareHandler : public MiddlewareHandler {
 
 class WebServerBase final {
  public:
+  // The AsyncWebServer is created once and intentionally never deleted: on Arduino
+  // platforms ESPAsyncWebServer owns its registered handlers, so destroying it would
+  // also destroy live components (e.g. the captive portal) out from under us.
+  // init()/deinit() refcount users and start/stop the listener; handlers are
+  // registered once at creation and survive listener restarts.
   void init() {
-    if (this->initialized_) {
-      this->initialized_++;
+    this->initialized_++;
+    if (this->server_ != nullptr) {
+      if (this->initialized_ == 1) {
+        // Restart the listener after a previous deinit()
+        this->server_->begin();
+      }
       return;
     }
     this->server_ = new AsyncWebServer(this->port_);
@@ -126,14 +135,13 @@ class WebServerBase final {
 
     for (auto *handler : this->handlers_)
       this->server_->addHandler(handler);
-
-    this->initialized_++;
   }
   void deinit() {
+    if (this->initialized_ == 0)
+      return;  // unbalanced deinit()
     this->initialized_--;
     if (this->initialized_ == 0) {
-      delete this->server_;
-      this->server_ = nullptr;
+      this->server_->end();
     }
   }
   AsyncWebServer *get_server() const { return this->server_; }