diff --git a/homeassistant/components/usb/consumers.py b/homeassistant/components/usb/consumers.py
index 8dd32c97dda5..e58b4e363426 100644
--- a/homeassistant/components/usb/consumers.py
+++ b/homeassistant/components/usb/consumers.py
@@ -1,6 +1,6 @@
 """Attribution of serial ports to the integrations and apps using them."""
 
-from collections.abc import Mapping, Sequence
+from collections.abc import Iterator, Mapping, Sequence
 import os
 import re
 from typing import Any
@@ -156,14 +156,29 @@ async def _async_get_config_entry_consumers(
     return consumers
 
 
+def _iter_option_device_paths(value: Any) -> Iterator[str]:
+    """Yield device paths configured anywhere in the options of an app."""
+    if isinstance(value, str):
+        if value.startswith("/dev/"):
+            yield value
+    elif isinstance(value, Mapping):
+        for item in value.values():
+            yield from _iter_option_device_paths(item)
+    elif isinstance(value, list):
+        for item in value:
+            yield from _iter_option_device_paths(item)
+
+
 @callback
 def _async_get_app_consumers(
     hass: HomeAssistant,
 ) -> dict[str, list[SerialPortConsumer]]:
-    """Return devices mapped into apps, either statically or through options.
+    """Return devices configured in the options of apps.
 
-    Supervisor resolves `device(subsystem=tty)` options into real devices, so device
-    paths that no longer exist are missing and non-serial devices are included.
+    The `devices` field of an app also lists the static devices of its manifest,
+    which are mapped into the container whether the app uses them or not, so only
+    options are evidence of a device being used. Options can refer to devices
+    that no longer exist or are not serial ports.
     """
     if not is_hassio(hass):
         return {}
@@ -179,7 +194,7 @@ def _async_get_app_consumers(
         if info is None:
             continue
 
-        for device in info["devices"]:
+        for device in _iter_option_device_paths(info["options"]):
             consumers.setdefault(device, []).append(
                 SerialPortConsumer(
                     kind="app",
@@ -224,7 +239,7 @@ async def async_get_serial_port_consumers(
         consumers.setdefault(device, []).extend(path_consumers)
 
     for path, path_consumers in app_consumers.items():
-        # Apps also map non-serial devices, only scanned ports are of interest
+        # Options can name non-serial devices, only scanned ports are of interest
         resolved_path = resolved[path]
 
         if resolved_path not in aliases:
diff --git a/tests/components/usb/test_consumers.py b/tests/components/usb/test_consumers.py
index e130bb46edcd..d00993f11834 100644
--- a/tests/components/usb/test_consumers.py
+++ b/tests/components/usb/test_consumers.py
@@ -439,17 +439,26 @@ async def test_app_consumers(
     hass: HomeAssistant,
     hass_ws_client: WebSocketGenerator,
 ) -> None:
-    """Test detecting serial ports mapped into apps."""
+    """Test detecting serial ports configured in the options of apps."""
     apps_info = {
         "core_zwave_js": {
             "name": "Z-Wave JS",
             "state": "started",
-            "devices": [TTY_USB0_BY_ID, "/dev/dri/card0"],
+            "devices": [TTY_USB0],
+            "options": {"device": TTY_USB0_BY_ID, "gpu": "/dev/dri/card0"},
         },
         "some_app": {
             "name": "Some App",
             "state": "stopped",
             "devices": [TTY_USB1],
+            "options": {"serial": [{"port": TTY_USB0}]},
+        },
+        # Static devices of the manifest are mapped regardless of being used
+        "wmbusmeters": {
+            "name": "Wmbusmeters",
+            "state": "started",
+            "devices": [TTY_USB0, TTY_USB1],
+            "options": {"reset_config": False},
         },
         "uninstalled_app": None,
     }
@@ -478,7 +487,15 @@ async def test_app_consumers(
                     "domain": None,
                     "config_entry_id": None,
                     "slug": "core_zwave_js",
-                }
+                },
+                {
+                    "kind": "app",
+                    "title": "Some App",
+                    "active": False,
+                    "domain": None,
+                    "config_entry_id": None,
+                    "slug": "some_app",
+                },
             ],
         ),
         (ESPHOME_PORT, []),
@@ -531,7 +548,12 @@ async def test_multiple_consumers(
     entry.add_to_hass(hass)
 
     apps_info = {
-        "some_app": {"name": "Some App", "state": "started", "devices": [TTY_USB0]}
+        "some_app": {
+            "name": "Some App",
+            "state": "started",
+            "devices": [TTY_USB0],
+            "options": {"device": TTY_USB0},
+        }
     }
 
     with (