diff --git a/esphome/components/api/__init__.py b/esphome/components/api/__init__.py
index 3568318dad..6202e127bf 100644
--- a/esphome/components/api/__init__.py
+++ b/esphome/components/api/__init__.py
@@ -14,6 +14,7 @@ from esphome.components.noise import (  # noqa: F401
     ENCRYPTION_SCHEMA,
     decode_encryption_key,
     encryption_schema,
+    new_psk_progmem,
     validate_encryption_key,
 )
 from esphome.config_helpers import filter_source_files_from_defines, get_logger_level
@@ -589,8 +590,7 @@ async def to_code(config: ConfigType) -> None:
 
     if (encryption_config := config.get(CONF_ENCRYPTION, None)) is not None:
         if key := encryption_config.get(CONF_KEY):
-            decoded = decode_encryption_key(key)
-            cg.add(var.set_noise_psk(list(decoded)))
+            cg.add(var.set_noise_psk(new_psk_progmem(config[CONF_ID], key)))
             cg.add_define("USE_API_NOISE_PSK_FROM_YAML")
         else:
             # No key provided, but encryption desired
diff --git a/esphome/components/api/api_frame_helper_noise.cpp b/esphome/components/api/api_frame_helper_noise.cpp
index 138dbdddba..29b2858aee 100644
--- a/esphome/components/api/api_frame_helper_noise.cpp
+++ b/esphome/components/api/api_frame_helper_noise.cpp
@@ -548,7 +548,7 @@ APIError APINoiseFrameHelper::write_frame_(const uint8_t *data, uint16_t len) {
  * @return 0 on success, -1 on error (check errno)
  */
 APIError APINoiseFrameHelper::init_handshake_() {
-  int err = this->handshake_.init(this->ctx_.get_psk(), prologue_.data(), prologue_.size());
+  int err = this->handshake_.init(this->ctx_, prologue_.data(), prologue_.size());
   APIError aerr = handle_noise_error_(err, LOG_STR("noise_handshake_init"), APIError::HANDSHAKESTATE_SETUP_FAILED);
   if (aerr != APIError::OK)
     return aerr;
diff --git a/esphome/components/api/api_server.cpp b/esphome/components/api/api_server.cpp
index 43d35363d3..f9069ab5c0 100644
--- a/esphome/components/api/api_server.cpp
+++ b/esphome/components/api/api_server.cpp
@@ -583,11 +583,14 @@ bool APIServer::update_noise_psk_(const SavedNoisePsk &new_psk, const LogString
 }
 
 bool APIServer::load_and_apply_noise_psk_() {
-  SavedNoisePsk saved{};
-  if (!this->noise_pref_.load(&saved))
+#ifdef USE_API_NOISE_PSK_FROM_YAML
+  return false;
+#else
+  if (!this->noise_pref_.load(&this->saved_psk_))
     return false;
-  this->set_noise_psk(saved.psk);
+  this->noise_ctx_.set_psk(this->saved_psk_.psk.data());
   return true;
+#endif
 }
 
 bool APIServer::save_noise_psk(noise::psk_t psk, bool make_active) {
@@ -597,8 +600,7 @@ bool APIServer::save_noise_psk(noise::psk_t psk, bool make_active) {
   ESP_LOGW(TAG, "Key set in YAML");
   return false;
 #else
-  auto &old_psk = this->noise_ctx_.get_psk();
-  if (std::equal(old_psk.begin(), old_psk.end(), psk.begin())) {
+  if (this->saved_psk_.psk == psk) {
     ESP_LOGW(TAG, "New PSK matches old");
     return true;
   }
diff --git a/esphome/components/api/api_server.h b/esphome/components/api/api_server.h
index 146ff09381..d5d9a357aa 100644
--- a/esphome/components/api/api_server.h
+++ b/esphome/components/api/api_server.h
@@ -78,7 +78,8 @@ class APIServer final : public Component,
 #ifdef USE_API_NOISE
   bool save_noise_psk(noise::psk_t psk, bool make_active = true);
   bool clear_noise_psk(bool make_active = true);
-  void set_noise_psk(const noise::psk_t &psk) { this->noise_ctx_.set_psk(psk); }
+  /// psk points at 32 bytes that live in flash for the life of the program
+  void set_noise_psk(const uint8_t *psk) { this->noise_ctx_.set_psk(psk); }
   noise::NoiseContext &get_noise_ctx() { return this->noise_ctx_; }
 #endif  // USE_API_NOISE
 
@@ -358,6 +359,9 @@ class APIServer final : public Component,
 
 #ifdef USE_API_NOISE
   noise::NoiseContext noise_ctx_;
+#ifndef USE_API_NOISE_PSK_FROM_YAML
+  SavedNoisePsk saved_psk_{};  // backs noise_ctx_ for a runtime provisioned key
+#endif
   ESPPreferenceObject noise_pref_;
 #endif  // USE_API_NOISE
 };
diff --git a/esphome/components/esphome/ota/__init__.py b/esphome/components/esphome/ota/__init__.py
index 6559000229..f2c37155ae 100644
--- a/esphome/components/esphome/ota/__init__.py
+++ b/esphome/components/esphome/ota/__init__.py
@@ -1,11 +1,7 @@
 import logging
 
 import esphome.codegen as cg
-from esphome.components.noise import (
-    decode_encryption_key,
-    encryption_schema,
-    is_reserved_key,
-)
+from esphome.components.noise import encryption_schema, is_reserved_key, new_psk_progmem
 from esphome.components.ota import BASE_OTA_SCHEMA, OTAComponent, ota_to_code
 from esphome.config_helpers import filter_source_files_from_defines, merge_config
 import esphome.config_validation as cv
@@ -25,7 +21,7 @@ from esphome.const import (
     CONF_VERSION,
     CONF_WEB_SERVER,
 )
-from esphome.core import CORE, ID, coroutine_with_priority
+from esphome.core import CORE, coroutine_with_priority
 from esphome.coroutine import CoroPriority
 import esphome.final_validate as fv
 from esphome.types import ConfigType
@@ -41,7 +37,8 @@ DEPENDENCIES = ["network"]
 
 
 def AUTO_LOAD(config: ConfigType) -> list[str]:
-    """Auto-load noise only when encryption is configured."""
+    """Auto-load noise only when encryption is configured. The api key offer
+    path inherits noise from the api component's own AUTO_LOAD."""
     base = ["sha256", "socket"]
     # A falsy config is a tooling probe for the maximal set (None from
     # dependency resolution, {} from the components-graph platform probe);
@@ -309,13 +306,7 @@ async def to_code(config: ConfigType) -> None:
         key = _api_static_key(CORE.config.get(CONF_API) or {})
     if key is not None:
         cg.add_define("USE_OTA_ENCRYPTION")
-        # The key stays in flash; it is copied into the handshake only while
-        # an encrypted session is open
-        psk = cg.progmem_array(
-            ID(f"{config[CONF_ID].id}_psk", is_declaration=True, type=cg.uint8),
-            list(decode_encryption_key(key)),
-        )
-        cg.add(var.set_noise_psk(psk))
+        cg.add(var.set_noise_psk(new_psk_progmem(config[CONF_ID], key)))
 
     # Build flag so lwip_fast_select.c (a .c file that can't include defines.h) sees it.
     cg.add_build_flag("-DUSE_OTA_PLATFORM_ESPHOME")
diff --git a/esphome/components/esphome/ota/ota_esphome.h b/esphome/components/esphome/ota/ota_esphome.h
index 9f7f6ae649..847ee34d40 100644
--- a/esphome/components/esphome/ota/ota_esphome.h
+++ b/esphome/components/esphome/ota/ota_esphome.h
@@ -46,7 +46,7 @@ class ESPHomeOTAComponent final : public ota::OTAComponent {
 
 #ifdef USE_OTA_ENCRYPTION
   /// psk points at 32 bytes that live in flash for the life of the program
-  void set_noise_psk(const uint8_t *psk) { this->noise_psk_ = psk; }
+  void set_noise_psk(const uint8_t *psk) { this->noise_ctx_.set_psk(psk); }
 #endif
 
   /// Manually set the port OTA should listen on
@@ -146,7 +146,7 @@ class ESPHomeOTAComponent final : public ota::OTAComponent {
   std::unique_ptr<uint8_t[]> auth_buf_;
 #endif  // USE_OTA_PASSWORD
 #ifdef USE_OTA_ENCRYPTION
-  const uint8_t *noise_psk_{nullptr};
+  noise::NoiseContext noise_ctx_;
   std::unique_ptr<NoiseSession> noise_;
 #endif  // USE_OTA_ENCRYPTION
 
diff --git a/esphome/components/esphome/ota/ota_esphome_noise.cpp b/esphome/components/esphome/ota/ota_esphome_noise.cpp
index 4e2abe4416..a9ed552211 100644
--- a/esphome/components/esphome/ota/ota_esphome_noise.cpp
+++ b/esphome/components/esphome/ota/ota_esphome_noise.cpp
@@ -65,15 +65,8 @@ bool ESPHomeOTAComponent::noise_start_session_(uint8_t server_feature_flags) {
   *p++ = ota::OTA_RESPONSE_FEATURE_FLAGS;
   *p++ = server_feature_flags;
 
-  // noise-c keeps its own copy of the key, so the flash copy is only read here
-  noise::psk_t psk;
-#ifdef USE_ESP8266
-  memcpy_P(psk.data(), this->noise_psk_, psk.size());
-#else
-  std::memcpy(psk.data(), this->noise_psk_, psk.size());
-#endif
-  int err =
-      this->noise_ == nullptr ? NOISE_ERROR_NO_MEMORY : this->noise_->handshake.init(psk, prologue, sizeof(prologue));
+  int err = this->noise_ == nullptr ? NOISE_ERROR_NO_MEMORY
+                                    : this->noise_->handshake.init(this->noise_ctx_, prologue, sizeof(prologue));
   if (err != 0) {
     ESP_LOGW(TAG, "Session init: %d", err);
     this->cleanup_connection_();
diff --git a/esphome/components/noise/__init__.py b/esphome/components/noise/__init__.py
index 0f9328a482..15b62a8ca0 100644
--- a/esphome/components/noise/__init__.py
+++ b/esphome/components/noise/__init__.py
@@ -5,6 +5,8 @@ from typing import Any
 import esphome.codegen as cg
 import esphome.config_validation as cv
 from esphome.const import CONF_KEY
+from esphome.core import ID
+from esphome.cpp_generator import MockObj
 from esphome.types import ConfigType
 
 CODEOWNERS = ["@esphome/core"]
@@ -61,6 +63,15 @@ ENCRYPTION_SCHEMA = cv.Schema(
 )
 
 
+def new_psk_progmem(parent_id: ID, key: str) -> MockObj:
+    """Emit the decoded key as a PROGMEM array; the component keeps a pointer
+    so the key never occupies RAM."""
+    return cg.progmem_array(
+        ID(f"{parent_id.id}_psk", is_declaration=True, type=cg.uint8),
+        list(decode_encryption_key(key)),
+    )
+
+
 def encryption_schema(config: ConfigType | None) -> ConfigType:
     # A bare `encryption:` block is valid; a missing key means the consumer
     # falls back to its keyless behavior (api provisioning, ota inheriting
diff --git a/esphome/components/noise/noise.cpp b/esphome/components/noise/noise.cpp
index 7c79e98098..54c1bb315b 100644
--- a/esphome/components/noise/noise.cpp
+++ b/esphome/components/noise/noise.cpp
@@ -15,9 +15,25 @@ namespace esphome::noise {
 
 static const char *const TAG = "noise";
 
-void NoiseContext::set_psk(const psk_t &psk) {
+void NoiseContext::set_psk(const uint8_t *psk) {
   this->psk_ = psk;
-  this->has_psk_ = !is_all_zeros(psk);
+  psk_t copy;
+  this->load_psk(copy);
+  if (is_all_zeros(copy)) {
+    this->psk_ = nullptr;
+  }
+}
+
+void NoiseContext::load_psk(psk_t &out) const {
+  if (this->psk_ == nullptr) {
+    out.fill(0);
+    return;
+  }
+#ifdef USE_ESP8266
+  memcpy_P(out.data(), this->psk_, out.size());
+#else
+  std::memcpy(out.data(), this->psk_, out.size());
+#endif
 }
 
 const LogString *noise_err_to_logstr(int err) {
diff --git a/esphome/components/noise/noise.h b/esphome/components/noise/noise.h
index 1e779f0380..9472414bbe 100644
--- a/esphome/components/noise/noise.h
+++ b/esphome/components/noise/noise.h
@@ -23,13 +23,16 @@ class NoiseContext {
     }
     return acc == 0;
   }
-  void set_psk(const psk_t &psk);
-  const psk_t &get_psk() const { return this->psk_; }
-  bool has_psk() const { return this->has_psk_; }
+  /// psk points at 32 bytes that outlive the context: a PROGMEM array from
+  /// codegen, or RAM owned by the caller for a runtime provisioned key.
+  /// The all-zeros key counts as no key.
+  void set_psk(const uint8_t *psk);
+  /// Copy the key out (flash-aware on ESP8266); all zeros when none is set.
+  void load_psk(psk_t &out) const;
+  bool has_psk() const { return this->psk_ != nullptr; }
 
  protected:
-  psk_t psk_{};
-  bool has_psk_{false};
+  const uint8_t *psk_{nullptr};
 };
 
 /// Convert a noise error code to a readable error
diff --git a/esphome/components/noise/noise_handshake.cpp b/esphome/components/noise/noise_handshake.cpp
index 6d426de012..cc7fa603c4 100644
--- a/esphome/components/noise/noise_handshake.cpp
+++ b/esphome/components/noise/noise_handshake.cpp
@@ -20,7 +20,7 @@ NoiseResponderHandshake::~NoiseResponderHandshake() {
   }
 }
 
-int NoiseResponderHandshake::init(const psk_t &psk, const uint8_t *prologue, size_t prologue_len) {
+int NoiseResponderHandshake::init(const NoiseContext &ctx, const uint8_t *prologue, size_t prologue_len) {
   if (this->handshake_ != nullptr) {
     noise_handshakestate_free(this->handshake_);
     this->handshake_ = nullptr;
@@ -44,6 +44,9 @@ int NoiseResponderHandshake::init(const psk_t &psk, const uint8_t *prologue, siz
     HANDSHAKE_STEP_LOG("noise_handshakestate_new_by_id", err);
     return err;
   }
+  // noise-c keeps its own copy, so the key only passes through the stack here
+  psk_t psk;
+  ctx.load_psk(psk);
   err = noise_handshakestate_set_pre_shared_key(this->handshake_, psk.data(), psk.size());
   if (err != 0) {
     HANDSHAKE_STEP_LOG("noise_handshakestate_set_pre_shared_key", err);
diff --git a/esphome/components/noise/noise_handshake.h b/esphome/components/noise/noise_handshake.h
index 30596f35c2..bf1aa8cb7f 100644
--- a/esphome/components/noise/noise_handshake.h
+++ b/esphome/components/noise/noise_handshake.h
@@ -36,9 +36,9 @@ class NoiseResponderHandshake {
   NoiseResponderHandshake(const NoiseResponderHandshake &) = delete;
   NoiseResponderHandshake &operator=(const NoiseResponderHandshake &) = delete;
 
-  /// Create and start the handshake with the given PSK and prologue. A
-  /// repeated call frees the previous handshake state and starts over.
-  [[nodiscard]] int init(const psk_t &psk, const uint8_t *prologue, size_t prologue_len);
+  /// Create and start the handshake with the context's PSK and the prologue.
+  /// A repeated call frees the previous handshake state and starts over.
+  [[nodiscard]] int init(const NoiseContext &ctx, const uint8_t *prologue, size_t prologue_len);
   /// ACTION_FAILED is the catch-all: returned before init(), after split()
   /// has released the state, and when noise-c reports a failed handshake.
   [[nodiscard]] Action action() const;
diff --git a/esphome/espota2.py b/esphome/espota2.py
index 40adb4527a..2d490caf99 100644
--- a/esphome/espota2.py
+++ b/esphome/espota2.py
@@ -539,10 +539,11 @@ def perform_ota(
                 "offer encryption; refusing to send the image in plaintext. "
                 "The running firmware was built before OTA encryption "
                 "(ESPHome 2026.9.0) or without an 'api: encryption: key'. "
-                "Firmware built with an api key offers encryption: install "
-                "once with the 'ota: encryption:' block removed, then restore "
-                "the block and install again. Otherwise flash by serial or "
-                "the web_server OTA platform."
+                "If the config has an 'api: encryption: key', install once "
+                "with the 'ota: encryption:' block removed (that firmware "
+                "offers encryption), then restore the block and install "
+                "again. Otherwise flash by serial or the web_server OTA "
+                "platform."
             )
         # The prologue binds every negotiation byte both sides saw, so any
         # tampering with the plaintext preamble breaks the handshake.
diff --git a/tests/components/noise/test_noise_handshake.cpp b/tests/components/noise/test_noise_handshake.cpp
index d879a26c43..f2081f2965 100644
--- a/tests/components/noise/test_noise_handshake.cpp
+++ b/tests/components/noise/test_noise_handshake.cpp
@@ -68,6 +68,14 @@ class Initiator {
 
 static const uint8_t PROLOGUE[] = {'t', 'e', 's', 't', 'p', 'r', 'o', 'l', 'o', 'g', 'u', 'e'};
 
+// The context only points at the key and init() copies it before returning,
+// so a temporary context over a temporary key is safe within one call
+static NoiseContext ctx_for(const psk_t &psk) {
+  NoiseContext ctx;
+  ctx.set_psk(psk.data());
+  return ctx;
+}
+
 static psk_t make_psk(uint8_t seed) {
   psk_t psk;
   for (size_t i = 0; i < psk.size(); i++) {
@@ -102,7 +110,7 @@ TEST(NoiseResponderHandshakeTest, MessageMethodsErrorBeforeInit) {
 TEST(NoiseResponderHandshakeTest, FullHandshakeAndTransportRoundTrip) {
   const psk_t psk = make_psk(7);
   NoiseResponderHandshake responder;
-  ASSERT_EQ(responder.init(psk, PROLOGUE, sizeof(PROLOGUE)), 0);
+  ASSERT_EQ(responder.init(ctx_for(psk), PROLOGUE, sizeof(PROLOGUE)), 0);
   EXPECT_EQ(responder.action(), Action::ACTION_READ);
 
   Initiator initiator(psk, PROLOGUE, sizeof(PROLOGUE));
@@ -155,8 +163,8 @@ TEST(NoiseResponderHandshakeTest, ReInitRestartsHandshake) {
   // proves the restart took effect; the old state surviving would fail the
   // MAC here.
   NoiseResponderHandshake responder;
-  ASSERT_EQ(responder.init(make_psk(7), PROLOGUE, sizeof(PROLOGUE)), 0);
-  ASSERT_EQ(responder.init(make_psk(9), PROLOGUE, sizeof(PROLOGUE)), 0);
+  ASSERT_EQ(responder.init(ctx_for(make_psk(7)), PROLOGUE, sizeof(PROLOGUE)), 0);
+  ASSERT_EQ(responder.init(ctx_for(make_psk(9)), PROLOGUE, sizeof(PROLOGUE)), 0);
   EXPECT_EQ(responder.action(), Action::ACTION_READ);
 
   Initiator initiator(make_psk(9), PROLOGUE, sizeof(PROLOGUE));
@@ -168,7 +176,7 @@ TEST(NoiseResponderHandshakeTest, ReInitRestartsHandshake) {
 
 TEST(NoiseResponderHandshakeTest, WrongPskFailsWithMacFailure) {
   NoiseResponderHandshake responder;
-  ASSERT_EQ(responder.init(make_psk(7), PROLOGUE, sizeof(PROLOGUE)), 0);
+  ASSERT_EQ(responder.init(ctx_for(make_psk(7)), PROLOGUE, sizeof(PROLOGUE)), 0);
 
   Initiator initiator(make_psk(200), PROLOGUE, sizeof(PROLOGUE));
   uint8_t msg[MAX_HANDSHAKE_SIZE];
@@ -185,7 +193,7 @@ TEST(NoiseResponderHandshakeTest, MismatchedPrologueFailsWithMacFailure) {
   // tampered preamble must fail even with the right key.
   const psk_t psk = make_psk(7);
   NoiseResponderHandshake responder;
-  ASSERT_EQ(responder.init(psk, PROLOGUE, sizeof(PROLOGUE)), 0);
+  ASSERT_EQ(responder.init(ctx_for(psk), PROLOGUE, sizeof(PROLOGUE)), 0);
 
   static const uint8_t TAMPERED[] = {'x'};
   Initiator initiator(psk, TAMPERED, sizeof(TAMPERED));
diff --git a/tests/components/noise/test_noise_primitives.cpp b/tests/components/noise/test_noise_primitives.cpp
index 018be9f717..2e89fbc682 100644
--- a/tests/components/noise/test_noise_primitives.cpp
+++ b/tests/components/noise/test_noise_primitives.cpp
@@ -17,12 +17,16 @@ TEST(NoiseContextTest, AllZerosPskIsReserved) {
   EXPECT_FALSE(NoiseContext::is_all_zeros(psk));
 
   NoiseContext ctx;
+  psk_t loaded;
   EXPECT_FALSE(ctx.has_psk());
-  ctx.set_psk(zeros);
+  ctx.load_psk(loaded);
+  EXPECT_EQ(loaded, zeros);
+  ctx.set_psk(zeros.data());
   EXPECT_FALSE(ctx.has_psk());
-  ctx.set_psk(psk);
+  ctx.set_psk(psk.data());
   EXPECT_TRUE(ctx.has_psk());
-  EXPECT_EQ(ctx.get_psk(), psk);
+  ctx.load_psk(loaded);
+  EXPECT_EQ(loaded, psk);
 }
 
 TEST(WireFormatTest, FrameHeaderIsIndicatorPlusBigEndianLength) {
diff --git a/tests/integration/test_host_ota.py b/tests/integration/test_host_ota.py
index 1f44c2253d..03158ae769 100644
--- a/tests/integration/test_host_ota.py
+++ b/tests/integration/test_host_ota.py
@@ -143,25 +143,13 @@ async def test_host_ota_encrypted(
             pid_before = proc.pid
 
             # A plaintext upload must be refused with the device unharmed
-            rc, _ = await loop.run_in_executor(
-                None, espota2.run_ota, LOCALHOST, ota_port, None, binary_path
-            )
+            rc = await _run_ota(ota_port, None, binary_path, None)
             assert rc == 1, "plaintext upload to an encrypted device must fail"
             await asyncio.sleep(0.5)
             assert proc.returncode is None, "process died on rejected plaintext OTA"
 
             # The encrypted upload goes through and the device re-execs
-            rc, _ = await loop.run_in_executor(
-                None,
-                functools.partial(
-                    espota2.run_ota,
-                    LOCALHOST,
-                    ota_port,
-                    None,
-                    binary_path,
-                    noise_psk=API_KEY,
-                ),
-            )
+            rc = await _run_ota(ota_port, None, binary_path, API_KEY)
             assert rc == 0, "encrypted OTA reported failure"
             await asyncio.wait_for(rebooted, timeout=10.0)
             await _wait_for_port(LOCALHOST, api_port, PORT_WAIT_TIMEOUT)