diff --git a/esphome/core/config.py b/esphome/core/config.py
index b925f0b7d9..59c96035b8 100644
--- a/esphome/core/config.py
+++ b/esphome/core/config.py
@@ -407,6 +407,17 @@ def preload_core_config(config, result) -> str:
 
     CORE.name = conf[CONF_NAME]
     CORE.friendly_name = conf.get(CONF_FRIENDLY_NAME)
+    # Record the node's area name now (substitutions are already resolved at this
+    # point). storage.json is written before to_code() runs, so deferring this to
+    # to_code() left the area as null in storage.json. The value here is the raw
+    # post-substitution form (a plain string or a {name: ...} mapping). Assign
+    # unconditionally (like friendly_name) so a config without an area never
+    # inherits a stale value from a previous load in a long-running process, and
+    # use .get() so a malformed mapping surfaces later as a proper validation
+    # error rather than a KeyError here. to_code() sets it again from the
+    # validated config, which yields the same name.
+    area = conf.get(CONF_AREA)
+    CORE.area = area.get(CONF_NAME) if isinstance(area, dict) else area
     CORE.data[KEY_CORE] = {}
 
     if CONF_BUILD_PATH not in conf:
@@ -760,7 +771,6 @@ async def to_code(config: ConfigType) -> None:
     # Process areas
     all_areas: list[dict[str, str | core.ID]] = []
     if CONF_AREA in config:
-        CORE.area = config[CONF_AREA][CONF_NAME]
         all_areas.append(config[CONF_AREA])
     all_areas.extend(config[CONF_AREAS])
 
diff --git a/tests/unit_tests/core/test_config.py b/tests/unit_tests/core/test_config.py
index e2b34d92d8..b3d87f6857 100644
--- a/tests/unit_tests/core/test_config.py
+++ b/tests/unit_tests/core/test_config.py
@@ -152,15 +152,21 @@ def test_multiple_areas_and_devices(yaml_file: Callable[[str], str]) -> None:
         ("multiple_areas_devices.yaml", "Main Area"),
     ],
 )
-async def test_to_code_records_core_area(
+async def test_core_area_recorded_at_config_load(
     yaml_file: Callable[[str], Path],
     fixture: str,
     expected_area: str,
 ) -> None:
-    """``to_code`` records the node's area name on CORE for StorageJSON."""
+    """The node's area name is recorded on CORE for StorageJSON.
+
+    It must be set during config load (preload_core_config), not deferred to
+    to_code(): storage.json is written before to_code() runs, so a late
+    assignment left the area as null in storage.json (regression #17218).
+    """
     result = load_config_from_fixture(yaml_file, fixture, FIXTURES_DIR)
     assert result is not None
-    assert CORE.area is None
+    # Recorded already at config-load time, before any code generation.
+    assert CORE.area == expected_area
 
     with patch("esphome.core.config.cg") as mock_cg:
         mock_cg.RawStatement.side_effect = lambda *args, **kwargs: MagicMock()
@@ -170,6 +176,23 @@ async def test_to_code_records_core_area(
     assert CORE.area == expected_area
 
 
+def test_config_load_without_area_clears_stale_core_area(
+    yaml_file: Callable[[str], Path],
+) -> None:
+    """A config without an area must not inherit a stale CORE.area.
+
+    preload_core_config assigns CORE.area unconditionally, so the area from a
+    previous load in a long-running process cannot leak into a config that
+    omits it.
+    """
+    CORE.area = "Stale Area From Previous Load"
+    result = load_config_from_fixture(
+        yaml_file, "device_without_area.yaml", FIXTURES_DIR
+    )
+    assert result is not None
+    assert CORE.area is None
+
+
 def test_legacy_string_area(
     yaml_file: Callable[[str], str], caplog: pytest.LogCaptureFixture
 ) -> None: