diff --git a/.changeset/eighty-taxis-wash.md b/.changeset/eighty-taxis-wash.md
new file mode 100644
index 0000000000..c89e7c7dea
--- /dev/null
+++ b/.changeset/eighty-taxis-wash.md
@@ -0,0 +1,8 @@
+---
+'@backstage/plugin-catalog-backend-module-github': patch
+'@backstage/plugin-catalog-backend-module-ldap': patch
+'@backstage/plugin-catalog-backend-module-msgraph': patch
+'@backstage/plugin-org': patch
+---
+
+Updated the code to handle User kind `spec.memberOf` now being optional.
diff --git a/.changeset/strong-dolphins-turn.md b/.changeset/strong-dolphins-turn.md
new file mode 100644
index 0000000000..4c59accba6
--- /dev/null
+++ b/.changeset/strong-dolphins-turn.md
@@ -0,0 +1,14 @@
+---
+'@backstage/catalog-model': minor
+---
+
+**BREAKING**: The User kind has an updated TypeScript type where `spec.memberOf`
+is optional.
+
+**NOTE HOWEVER**, that this only applies to the TypeScript types `UserEntity`
+and `UserEntityV1alpha1`. The catalog validation still requires the field to be
+set, even if it's in the form of an empty array. If you try to ingest data that
+stops producing this field, those entities _will be rejected_ by the catalog.
+The reason for these choices is that consumers will get a long grace period
+where old code still can rely on the underlying data being present, giving users
+ample time to update before actual breakages could happen.
diff --git a/packages/catalog-model/api-report.md b/packages/catalog-model/api-report.md
index 618c1f7b69..fca23d6ab9 100644
--- a/packages/catalog-model/api-report.md
+++ b/packages/catalog-model/api-report.md
@@ -447,7 +447,7 @@ interface UserEntityV1alpha1 extends Entity {
       email?: string;
       picture?: string;
     };
-    memberOf: string[];
+    memberOf?: string[];
   };
 }
 export { UserEntityV1alpha1 as UserEntity };
diff --git a/packages/catalog-model/src/kinds/UserEntityV1alpha1.ts b/packages/catalog-model/src/kinds/UserEntityV1alpha1.ts
index 82aaebd9d6..55c9b176ea 100644
--- a/packages/catalog-model/src/kinds/UserEntityV1alpha1.ts
+++ b/packages/catalog-model/src/kinds/UserEntityV1alpha1.ts
@@ -32,7 +32,7 @@ export interface UserEntityV1alpha1 extends Entity {
       email?: string;
       picture?: string;
     };
-    memberOf: string[];
+    memberOf?: string[];
   };
 }
 
diff --git a/plugins/catalog-backend-module-github/src/lib/org.ts b/plugins/catalog-backend-module-github/src/lib/org.ts
index 3c71f350e6..79a96b5e71 100644
--- a/plugins/catalog-backend-module-github/src/lib/org.ts
+++ b/plugins/catalog-backend-module-github/src/lib/org.ts
@@ -58,7 +58,10 @@ export function assignGroupsToUsers(
   for (const [groupName, userNames] of groupMemberUsers.entries()) {
     for (const userName of userNames) {
       const user = usersByName.get(userName);
-      if (user && !user.spec.memberOf.includes(groupName)) {
+      if (user && !user.spec.memberOf?.includes(groupName)) {
+        if (!user.spec.memberOf) {
+          user.spec.memberOf = [];
+        }
         user.spec.memberOf.push(groupName);
       }
     }
@@ -74,7 +77,7 @@ export function buildMemberOf(groups: GroupEntity[], users: UserEntity[]) {
     const transitiveMemberOf = new Set<string>();
 
     const todo = [
-      ...user.spec.memberOf,
+      ...(user.spec.memberOf ?? []),
       ...groups
         .filter(g => g.spec.members?.includes(user.metadata.name))
         .map(g => g.metadata.name),
diff --git a/plugins/catalog-backend-module-ldap/src/ldap/org.ts b/plugins/catalog-backend-module-ldap/src/ldap/org.ts
index fe59451a9d..28ccbd1d3b 100644
--- a/plugins/catalog-backend-module-ldap/src/ldap/org.ts
+++ b/plugins/catalog-backend-module-ldap/src/ldap/org.ts
@@ -61,7 +61,7 @@ export function buildMemberOf(groups: GroupEntity[], users: UserEntity[]) {
     const transitiveMemberOf = new Set<string>();
 
     const todo = [
-      ...user.spec.memberOf,
+      ...(user.spec.memberOf ?? []),
       ...groups
         .filter(g => g.spec.members?.includes(user.metadata.name))
         .map(g => g.metadata.name),
diff --git a/plugins/catalog-backend-module-msgraph/src/microsoftGraph/org.ts b/plugins/catalog-backend-module-msgraph/src/microsoftGraph/org.ts
index fe59451a9d..28ccbd1d3b 100644
--- a/plugins/catalog-backend-module-msgraph/src/microsoftGraph/org.ts
+++ b/plugins/catalog-backend-module-msgraph/src/microsoftGraph/org.ts
@@ -61,7 +61,7 @@ export function buildMemberOf(groups: GroupEntity[], users: UserEntity[]) {
     const transitiveMemberOf = new Set<string>();
 
     const todo = [
-      ...user.spec.memberOf,
+      ...(user.spec.memberOf ?? []),
       ...groups
         .filter(g => g.spec.members?.includes(user.metadata.name))
         .map(g => g.metadata.name),
diff --git a/plugins/catalog-backend-module-msgraph/src/microsoftGraph/read.ts b/plugins/catalog-backend-module-msgraph/src/microsoftGraph/read.ts
index 7174a6012c..e9760f7698 100644
--- a/plugins/catalog-backend-module-msgraph/src/microsoftGraph/read.ts
+++ b/plugins/catalog-backend-module-msgraph/src/microsoftGraph/read.ts
@@ -507,6 +507,9 @@ export function resolveRelations(
     retrieveItems(groupMemberOf, id).forEach(p => {
       const parentGroup = groupMap.get(p);
       if (parentGroup) {
+        if (!user.spec.memberOf) {
+          user.spec.memberOf = [];
+        }
         user.spec.memberOf.push(stringifyEntityRef(parentGroup));
       }
     });
diff --git a/plugins/org/src/components/Cards/OwnershipCard/OwnershipCard.tsx b/plugins/org/src/components/Cards/OwnershipCard/OwnershipCard.tsx
index 8635d0d7d4..fb49843e92 100644
--- a/plugins/org/src/components/Cards/OwnershipCard/OwnershipCard.tsx
+++ b/plugins/org/src/components/Cards/OwnershipCard/OwnershipCard.tsx
@@ -118,7 +118,7 @@ const getQueryParams = (
   };
   if (owner.kind === 'User') {
     const user = owner as UserEntity;
-    filters.owners = [...filters.owners, ...user.spec.memberOf];
+    filters.owners = [...filters.owners, ...(user.spec.memberOf ?? [])];
   }
   const queryParams = qs.stringify(
     {