diff --git a/supervisor/addons/addon.py b/supervisor/addons/addon.py
index f08391b5d60..4bfbd5f4bbd 100644
--- a/supervisor/addons/addon.py
+++ b/supervisor/addons/addon.py
@@ -1682,8 +1682,9 @@ async def watchdog_container(self, event: DockerContainerStateEvent) -> None:
         ]:
             await self._restart_after_problem(event.state)
 
-    def refresh_path_cache(self) -> Awaitable[None]:
+    async def refresh_path_cache(self) -> None:
         """Refresh cache of existing paths."""
         if self.is_detached or not self.addon_store:
-            return super().refresh_path_cache()
-        return self.addon_store.refresh_path_cache()
+            await super().refresh_path_cache()
+        else:
+            await self.addon_store.refresh_path_cache()
diff --git a/supervisor/addons/model.py b/supervisor/addons/model.py
index c6ca928dacd..8b5cf1319b4 100644
--- a/supervisor/addons/model.py
+++ b/supervisor/addons/model.py
@@ -2,7 +2,7 @@
 
 from abc import ABC, abstractmethod
 from collections import defaultdict
-from collections.abc import Awaitable, Callable
+from collections.abc import Callable
 from contextlib import suppress
 from datetime import datetime
 import logging
@@ -91,6 +91,7 @@
 from ..coresys import CoreSys
 from ..docker.const import Capabilities
 from ..exceptions import (
+    AddonFileReadError,
     AddonNotSupportedArchitectureError,
     AddonNotSupportedError,
     AddonNotSupportedHomeAssistantVersionError,
@@ -682,9 +683,15 @@ def read_readme() -> str | None:
             # Return data
             return readme.read_text(encoding="utf-8", errors="replace")
 
-        return await self.sys_run_in_executor(read_readme)
-
-    def refresh_path_cache(self) -> Awaitable[None]:
+        try:
+            return await self.sys_run_in_executor(read_readme)
+        except OSError as err:
+            self.sys_resolution.check_oserror(err)
+            raise AddonFileReadError(
+                _LOGGER.error, addon=self.slug, error=str(err)
+            ) from err
+
+    async def refresh_path_cache(self) -> None:
         """Refresh cache of existing paths."""
 
         def check_paths():
@@ -693,7 +700,13 @@ def check_paths():
             self._path_changelog_exists = self.path_changelog.exists()
             self._path_documentation_exists = self.path_documentation.exists()
 
-        return self.sys_run_in_executor(check_paths)
+        try:
+            await self.sys_run_in_executor(check_paths)
+        except OSError as err:
+            self.sys_resolution.check_oserror(err)
+            raise AddonFileReadError(
+                _LOGGER.error, addon=self.slug, error=str(err)
+            ) from err
 
     def validate_availability(self) -> None:
         """Validate if addon is available for current system."""
diff --git a/supervisor/core.py b/supervisor/core.py
index 0f77bd3b992..29571d1f5b5 100644
--- a/supervisor/core.py
+++ b/supervisor/core.py
@@ -185,17 +185,32 @@ async def setup(self) -> None:
 
         # Execute each load task in secure context
         for setup_task in setup_loads:
+            unhealthy_before = self.sys_resolution.unhealthy.copy()
             try:
                 await setup_task
             except Exception as err:  # pylint: disable=broad-except
-                _LOGGER.critical(
-                    "Fatal error happening on load Task %s: %s",
-                    setup_task,
-                    err,
-                    exc_info=True,
-                )
+                # If the error already caused a new unhealthy reason to
+                # be set (e.g. via check_oserror), it was handled by the
+                # resolution system and the user has been notified. Skip
+                # capturing to Sentry in that case.
+                capture_exception = self.sys_resolution.unhealthy == unhealthy_before
+
                 self.sys_resolution.add_unhealthy_reason(UnhealthyReason.SETUP)
-                await async_capture_exception(err)
+
+                if capture_exception:
+                    _LOGGER.critical(
+                        "Fatal error happening on load Task %s: %s",
+                        setup_task,
+                        err,
+                        exc_info=True,
+                    )
+                    await async_capture_exception(err)
+                else:
+                    _LOGGER.error(
+                        "Error on load Task %s: %s",
+                        setup_task,
+                        err,
+                    )
 
     async def start(self) -> None:
         """Start Supervisor orchestration."""
diff --git a/supervisor/exceptions.py b/supervisor/exceptions.py
index 3b9415506cb..205293c7a45 100644
--- a/supervisor/exceptions.py
+++ b/supervisor/exceptions.py
@@ -561,6 +561,26 @@ def __init__(
         super().__init__(logger)
 
 
+class AddonFileReadError(AddonsError, APIError):
+    """Raise when an add-on metadata file cannot be read due to a filesystem error."""
+
+    error_key = "addon_file_read_error"
+    message_template = (
+        "Could not read metadata for add-on {addon} due to a filesystem error: {error}"
+    )
+
+    def __init__(
+        self,
+        logger: Callable[..., None] | None = None,
+        *,
+        addon: str,
+        error: str,
+    ) -> None:
+        """Initialize exception."""
+        self.extra_fields = {"addon": addon, "error": error}
+        super().__init__(None, logger)
+
+
 class AddonsJobError(AddonsError, JobException):
     """Raise on job errors."""