diff --git a/packages/manager/.changeset/pr-13547-fixed-1774943336443.md b/packages/manager/.changeset/pr-13547-fixed-1774943336443.md
new file mode 100644
index 00000000000..8e10d68ebcf
--- /dev/null
+++ b/packages/manager/.changeset/pr-13547-fixed-1774943336443.md
@@ -0,0 +1,5 @@
+---
+"@linode/manager": Fixed
+---
+
+Increase profile preferences reliability ([#13547](https://github.com/linode/manager/pull/13547))
diff --git a/packages/manager/src/components/PrimaryNav/PrimaryNav.tsx b/packages/manager/src/components/PrimaryNav/PrimaryNav.tsx
index 53566087f9f..5c791a53338 100644
--- a/packages/manager/src/components/PrimaryNav/PrimaryNav.tsx
+++ b/packages/manager/src/components/PrimaryNav/PrimaryNav.tsx
@@ -94,6 +94,20 @@ export interface PrimaryNavProps {
   isCollapsed: boolean;
 }
 
+/** Indices for product-family accordions when the user has not saved `collapsedSideNavProductFamilies` yet. */
+const DEFAULT_COLLAPSED_SIDE_NAV_INDICES = [1, 2, 3, 4, 5, 6, 7];
+
+function getActiveSideNavGroupIndex(
+  groups: ProductFamilyLinkGroup<PrimaryLinkType[]>[],
+  pathname: string
+) {
+  return groups.findIndex((group) => {
+    const filteredLinks = group.links.filter((link) => !link.hide);
+
+    return filteredLinks.some((link) => linkIsActive(pathname, link.to));
+  });
+}
+
 export const PrimaryNav = (props: PrimaryNavProps) => {
   const { closeMenu, desktopMenuToggle, isCollapsed } = props;
   const navItemsRef = React.useRef<HTMLDivElement>(null);
@@ -131,20 +145,11 @@ export const PrimaryNav = (props: PrimaryNavProps) => {
 
   const { isReserveIpEnabled } = useIsReserveIpEnabled();
 
-  const {
-    data: preferences,
-    error: preferencesError,
-    isLoading: preferencesLoading,
-  } = usePreferences();
+  const { data: preferences } = usePreferences();
 
   const collapsedSideNavPreference =
     preferences?.collapsedSideNavProductFamilies;
 
-  const collapsedAccordions = React.useMemo(
-    () => collapsedSideNavPreference ?? [1, 2, 3, 4, 5, 6, 7], // by default, we collapse all categories if no preference is set;
-    [collapsedSideNavPreference]
-  );
-
   const { mutateAsync: updatePreferences } = useMutatePreferences();
 
   const productFamilyLinkGroups: ProductFamilyLinkGroup<PrimaryLinkType[]>[] =
@@ -371,6 +376,30 @@ export const PrimaryNav = (props: PrimaryNavProps) => {
       ]
     );
 
+  const collapsedAccordions = React.useMemo(() => {
+    if (preferences === undefined) {
+      return DEFAULT_COLLAPSED_SIDE_NAV_INDICES;
+    }
+    if (collapsedSideNavPreference !== undefined) {
+      return collapsedSideNavPreference;
+    }
+    const activeGroupIndex = getActiveSideNavGroupIndex(
+      productFamilyLinkGroups,
+      location.pathname
+    );
+    if (activeGroupIndex === -1) {
+      return DEFAULT_COLLAPSED_SIDE_NAV_INDICES;
+    }
+    return DEFAULT_COLLAPSED_SIDE_NAV_INDICES.filter(
+      (idx) => idx !== activeGroupIndex
+    );
+  }, [
+    collapsedSideNavPreference,
+    preferences,
+    productFamilyLinkGroups,
+    location.pathname,
+  ]);
+
   const accordionClicked = React.useCallback(
     (index: number) => {
       let updatedCollapsedAccordions: number[];
@@ -434,48 +463,6 @@ export const PrimaryNav = (props: PrimaryNavProps) => {
     };
   }, [checkOverflow]);
 
-  // This effect will only run if the collapsedSideNavPreference is not set
-  // When a user lands on a page and does not have any preference set,
-  // we want to expand the accordion that contains the active link for convenience and discoverability
-  React.useEffect(() => {
-    // Wait for preferences to load or if there's an error
-    if (preferencesLoading || preferencesError) {
-      return;
-    }
-
-    // Wait for preferences data to be available (not just the field, but the whole object)
-    if (!preferences) {
-      return;
-    }
-
-    // If user has already set collapsedSideNavProductFamilies preference, don't override it
-    if (collapsedSideNavPreference) {
-      return;
-    }
-
-    // Find the index of the group containing the active link and expand it
-    const activeGroupIndex = productFamilyLinkGroups.findIndex((group) => {
-      const filteredLinks = group.links.filter((link) => !link.hide);
-
-      return filteredLinks.some((link) =>
-        linkIsActive(location.pathname, link.to)
-      );
-    });
-
-    if (activeGroupIndex !== -1) {
-      accordionClicked(activeGroupIndex);
-    }
-  }, [
-    accordionClicked,
-    location.pathname,
-    location.search,
-    productFamilyLinkGroups,
-    collapsedSideNavPreference,
-    preferences,
-    preferencesLoading,
-    preferencesError,
-  ]);
-
   let activeProductFamily = '';
 
   return (
diff --git a/packages/queries/src/profile/preferences.ts b/packages/queries/src/profile/preferences.ts
index cfcc9529f02..1f1f58baac8 100644
--- a/packages/queries/src/profile/preferences.ts
+++ b/packages/queries/src/profile/preferences.ts
@@ -1,5 +1,10 @@
 import { updateUserPreferences } from '@linode/api-v4';
-import { useMutation, useQuery, useQueryClient } from '@tanstack/react-query';
+import {
+  queryOptions,
+  useMutation,
+  useQuery,
+  useQueryClient,
+} from '@tanstack/react-query';
 
 import { queryPresets } from '../base';
 import { profileQueries } from './profile';
@@ -8,6 +13,14 @@ import type { APIError } from '@linode/api-v4';
 import type { ManagerPreferences } from '@linode/utilities';
 import type { QueryClient } from '@tanstack/react-query';
 
+const isPreferencesMergeBase = (
+  value: ManagerPreferences | undefined,
+): value is ManagerPreferences =>
+  value !== null &&
+  value !== undefined &&
+  typeof value === 'object' &&
+  !Array.isArray(value);
+
 // Reference for this pattern: https://tkdodo.eu/blog/react-query-data-transformations#3-using-the-select-option
 export const usePreferences = <TData = ManagerPreferences>(
   select?: (data: ManagerPreferences | undefined) => TData,
@@ -32,12 +45,17 @@ export const useMutatePreferences = (replace = false) => {
       if (replace) {
         return updateUserPreferences(data);
       }
-      const existingPreferences =
-        await queryClient.ensureQueryData<ManagerPreferences>(
-          profileQueries.preferences,
-        );
+      const preferencesQueryOptions = queryOptions(profileQueries.preferences);
+      const existingPreferences = await queryClient.ensureQueryData(
+        preferencesQueryOptions,
+      );
+
       return updateUserPreferences({ ...existingPreferences, ...data });
     },
+    onError: () =>
+      queryClient.invalidateQueries({
+        queryKey: profileQueries.preferences.queryKey,
+      }),
     onMutate: (data) => updatePreferenceData(data, replace, queryClient),
   });
 };
@@ -49,9 +67,14 @@ export const updatePreferenceData = (
 ): void => {
   queryClient.setQueryData<ManagerPreferences>(
     profileQueries.preferences.queryKey,
-    (oldData) => ({
-      ...(!replace ? oldData : {}),
-      ...newData,
-    }),
+    (oldData) => {
+      if (replace) {
+        return { ...newData };
+      }
+      if (!isPreferencesMergeBase(oldData)) {
+        return oldData;
+      }
+      return { ...oldData, ...newData };
+    },
   );
 };