diff --git a/esphome/components/wifi/__init__.py b/esphome/components/wifi/__init__.py
index 5879729a22b..6e75c57d1b2 100644
--- a/esphome/components/wifi/__init__.py
+++ b/esphome/components/wifi/__init__.py
@@ -259,6 +259,22 @@ WiFiConfigureAction = wifi_ns.class_(
 )
 
 
+# The supplicant parses the bootstrapping key as a DER encoded P-256 private key in hex; these wrap the
+# 32 byte key the way the ESP-IDF enrollee example does
+DPP_KEY_DER_PREFIX = "30310201010420"
+DPP_KEY_DER_SUFFIX = "a00a06082a8648ce3d030107"
+
+
+def _validate_dpp_private_key(value: object) -> str:
+    """The key is 32 bytes written as 64 hexadecimal characters."""
+    value = cv.string_strict(value)
+    if len(value) != 64 or any(c not in "0123456789abcdefABCDEF" for c in value):
+        raise cv.Invalid(
+            "private_key must be 32 bytes written as 64 hexadecimal characters"
+        )
+    return value.lower()
+
+
 def _validate_dpp_device_info(value: object) -> str:
     """The supplicant puts the text on a space separated command line and reads it up to the next space."""
     value = cv.string_strict(value)
@@ -336,7 +352,7 @@ EAP_AUTH_SCHEMA = cv.All(
 # Wi-Fi Easy Connect (DPP) enrollee; the ESP-IDF supplicant supports the QR code method
 DPP_SCHEMA = cv.Schema(
     {
-        cv.Optional(CONF_PRIVATE_KEY): cv.sensitive(cv.string_strict),
+        cv.Optional(CONF_PRIVATE_KEY): cv.sensitive(_validate_dpp_private_key),
         cv.Optional(CONF_DEVICE_INFO): _validate_dpp_device_info,
         cv.Optional(CONF_CHANNELS, default=[6]): cv.ensure_list(
             cv.int_range(min=1, max=14)
@@ -853,7 +869,7 @@ async def to_code(config):
         add_idf_sdkconfig_option("CONFIG_ESP_WIFI_DPP_SUPPORT", True)
         add_idf_sdkconfig_option("CONFIG_ESP_HOSTED_ENABLE_DPP", True)
         if (key := dpp.get(CONF_PRIVATE_KEY)) is not None:
-            cg.add(var.set_dpp_key(key))
+            cg.add(var.set_dpp_key(f"{DPP_KEY_DER_PREFIX}{key}{DPP_KEY_DER_SUFFIX}"))
         if (info := dpp.get(CONF_DEVICE_INFO)) is not None:
             cg.add(var.set_dpp_device_info(info))
         cg.add(var.set_dpp_channels(",".join(str(c) for c in dpp[CONF_CHANNELS])))
diff --git a/tests/component_tests/wifi/config/dpp_key.yaml b/tests/component_tests/wifi/config/dpp_key.yaml
new file mode 100644
index 00000000000..ba25f5e911e
--- /dev/null
+++ b/tests/component_tests/wifi/config/dpp_key.yaml
@@ -0,0 +1,12 @@
+---
+esphome:
+  name: test
+
+esp32:
+  board: esp32dev
+  framework:
+    type: esp-idf
+
+wifi:
+  dpp:
+    private_key: 00112233445566778899AABBCCDDEEFF00112233445566778899aabbccddeeff
diff --git a/tests/component_tests/wifi/test_dpp_key.py b/tests/component_tests/wifi/test_dpp_key.py
new file mode 100644
index 00000000000..96697dbb865
--- /dev/null
+++ b/tests/component_tests/wifi/test_dpp_key.py
@@ -0,0 +1,42 @@
+"""The DPP bootstrapping key is given as 32 raw bytes in hex and handed to the supplicant DER encoded."""
+
+from collections.abc import Callable
+from pathlib import Path
+
+import pytest
+
+from esphome.components import wifi
+import esphome.config_validation as cv
+
+RAW_KEY = "00112233445566778899aabbccddeeff00112233445566778899aabbccddeeff"
+
+
+@pytest.mark.parametrize(
+    "value",
+    [
+        RAW_KEY[:-2],
+        RAW_KEY + "00",
+        "zz" + RAW_KEY[2:],
+        wifi.DPP_KEY_DER_PREFIX + RAW_KEY + wifi.DPP_KEY_DER_SUFFIX,
+    ],
+)
+def test_key_must_be_64_hex_digits(value: str) -> None:
+    with pytest.raises(cv.Invalid, match="64 hexadecimal characters"):
+        wifi._validate_dpp_private_key(value)
+
+
+def test_key_is_lower_cased() -> None:
+    assert wifi._validate_dpp_private_key(RAW_KEY.upper()) == RAW_KEY
+
+
+def test_generated_key_is_der_encoded(
+    generate_main: Callable[[str | Path], str],
+    component_config_path: Callable[[str], Path],
+) -> None:
+    """The ESP-IDF supplicant expects the P-256 DER header around the raw key."""
+    main_cpp = generate_main(component_config_path("dpp_key.yaml"))
+
+    assert (
+        f'set_dpp_key("{wifi.DPP_KEY_DER_PREFIX}{RAW_KEY}{wifi.DPP_KEY_DER_SUFFIX}")'
+        in main_cpp
+    )
diff --git a/tests/components/wifi/test-dpp.esp32-idf.yaml b/tests/components/wifi/test-dpp.esp32-idf.yaml
index 29ec40ba797..1bd0d64fb5e 100644
--- a/tests/components/wifi/test-dpp.esp32-idf.yaml
+++ b/tests/components/wifi/test-dpp.esp32-idf.yaml
@@ -2,6 +2,7 @@ wifi:
   dpp:
     channels: [1, 6, 11]
     device_info: ESPHome
+    private_key: 00112233445566778899aabbccddeeff00112233445566778899aabbccddeeff
     timeout: 30s
   on_dpp_uri:
     - logger.log: