diff --git a/api/queries_issue.go b/api/queries_issue.go
index f09360152..701b92039 100644
--- a/api/queries_issue.go
+++ b/api/queries_issue.go
@@ -38,6 +38,7 @@ type Issue struct {
 	Comments         Comments
 	Author           Author
 	Assignees        Assignees
+	AssignedActors   AssignedActors
 	Labels           Labels
 	ProjectCards     ProjectCards
 	ProjectItems     ProjectItems
@@ -91,6 +92,22 @@ func (a Assignees) Logins() []string {
 	return logins
 }
 
+type AssignedActors struct {
+	Edges []struct {
+		Node Actor
+	}
+	TotalCount int
+}
+
+// TODO kw: Display names for actors with special display names.
+func (a AssignedActors) Logins() []string {
+	logins := make([]string, len(a.Edges))
+	for i, a := range a.Edges {
+		logins[i] = a.Node.Login
+	}
+	return logins
+}
+
 type Labels struct {
 	Nodes      []IssueLabel
 	TotalCount int
diff --git a/api/queries_repo.go b/api/queries_repo.go
index 93a32d80c..978e844c4 100644
--- a/api/queries_repo.go
+++ b/api/queries_repo.go
@@ -146,6 +146,13 @@ type GitHubUser struct {
 	Name  string `json:"name"`
 }
 
+// Actor is a superset of User and Bot
+// At the time of writing, it does not support Name.
+type Actor struct {
+	ID    string `json:"id"`
+	Login string `json:"login"`
+}
+
 // BranchRef is the branch name in a GitHub repository
 type BranchRef struct {
 	Name string `json:"name"`
@@ -674,13 +681,14 @@ func RepoFindForks(client *Client, repo ghrepo.Interface, limit int) ([]*Reposit
 }
 
 type RepoMetadataResult struct {
-	CurrentLogin    string
-	AssignableUsers []RepoAssignee
-	Labels          []RepoLabel
-	Projects        []RepoProject
-	ProjectsV2      []ProjectV2
-	Milestones      []RepoMilestone
-	Teams           []OrgTeam
+	CurrentLogin     string
+	AssignableUsers  []AssignableUser
+	AssignableActors []AssignableActor
+	Labels           []RepoLabel
+	Projects         []RepoProject
+	ProjectsV2       []ProjectV2
+	Milestones       []RepoMilestone
+	Teams            []OrgTeam
 }
 
 func (m *RepoMetadataResult) MembersToIDs(names []string) ([]string, error) {
@@ -688,12 +696,22 @@ func (m *RepoMetadataResult) MembersToIDs(names []string) ([]string, error) {
 	for _, assigneeLogin := range names {
 		found := false
 		for _, u := range m.AssignableUsers {
-			if strings.EqualFold(assigneeLogin, u.Login) {
-				ids = append(ids, u.ID)
+			if strings.EqualFold(assigneeLogin, u.Login()) {
+				ids = append(ids, u.ID())
 				found = true
 				break
 			}
 		}
+
+		// Look for ID in assignable actors if not found in assignable users
+		for _, a := range m.AssignableActors {
+			if strings.EqualFold(assigneeLogin, a.Login()) {
+				ids = append(ids, a.ID())
+				found = true
+				break
+			}
+		}
+
 		if !found {
 			return nil, fmt.Errorf("'%s' not found", assigneeLogin)
 		}
@@ -885,12 +903,13 @@ func (m *RepoMetadataResult) Merge(m2 *RepoMetadataResult) {
 }
 
 type RepoMetadataInput struct {
-	Assignees  bool
-	Reviewers  bool
-	Labels     bool
-	ProjectsV1 bool
-	ProjectsV2 bool
-	Milestones bool
+	Assignees      bool
+	ActorAssignees bool
+	Reviewers      bool
+	Labels         bool
+	ProjectsV1     bool
+	ProjectsV2     bool
+	Milestones     bool
 }
 
 // RepoMetadata pre-fetches the metadata for attaching to issues and pull requests
@@ -899,14 +918,51 @@ func RepoMetadata(client *Client, repo ghrepo.Interface, input RepoMetadataInput
 	var g errgroup.Group
 
 	if input.Assignees || input.Reviewers {
-		g.Go(func() error {
-			users, err := RepoAssignableUsers(client, repo)
-			if err != nil {
-				err = fmt.Errorf("error fetching assignees: %w", err)
+
+		if input.ActorAssignees {
+			g.Go(func() error {
+				actors, err := RepoAssignableActors(client, repo)
+				if err != nil {
+					err = fmt.Errorf("error fetching assignees: %w", err)
+				}
+				result.AssignableActors = actors
+				return err
+			})
+
+			// If reviewers are also requested, we still need to fetch the assignable users
+			// since commands use assignable users for reviewers too,
+			// but Actors are not supported for requesting review (need to confirm this).
+			// TODO KW: find out how to do this in the above query so we don't need to
+			// run two potentially expensive queries. When we fetch Actors, this
+			// should still return Users - Users are distinguishable from other Actors
+			// by having a name property. Maybe we can use the Name to filter out
+			// non-user Actors and populate the users list for reviewers based on
+			// that.
+			// Note: this only matters for `gh pr` flows, which currently does not
+			// request actor assignees, so we probably won't hit this until
+			// `gh pr` requests actor assignees.
+			if input.Reviewers {
+				g.Go(func() error {
+					users, err := RepoAssignableUsers(client, repo)
+					if err != nil {
+						err = fmt.Errorf("error fetching assignees: %w", err)
+					}
+					result.AssignableUsers = users
+					return err
+				})
 			}
-			result.AssignableUsers = users
-			return err
-		})
+		} else {
+			// Not using Actors, fetch legacy assignable users.
+			g.Go(func() error {
+				users, err := RepoAssignableUsers(client, repo)
+				if err != nil {
+					err = fmt.Errorf("error fetching assignees: %w", err)
+				}
+				result.AssignableUsers = users
+				return err
+			})
+		}
+
 	}
 
 	if input.Reviewers {
@@ -1070,12 +1126,16 @@ func RepoResolveMetadataIDs(client *Client, repo ghrepo.Interface, input RepoRes
 				result.Teams = append(result.Teams, t)
 			}
 		default:
-			user := RepoAssignee{}
+			user := struct {
+				Id    string
+				Login string
+				Name  string
+			}{}
 			err := json.Unmarshal(v, &user)
 			if err != nil {
 				return result, err
 			}
-			result.AssignableUsers = append(result.AssignableUsers, user)
+			result.AssignableUsers = append(result.AssignableUsers, NewAssignableUser(user.Id, user.Login, user.Name))
 		}
 	}
 
@@ -1127,26 +1187,84 @@ func RepoProjects(client *Client, repo ghrepo.Interface) ([]RepoProject, error)
 	return projects, nil
 }
 
-type RepoAssignee struct {
-	ID    string
-	Login string
-	Name  string
+type AssignableActor interface {
+	DisplayName() string
+	ID() string
+	Login() string
+
+	sealedAssignableActor()
+}
+
+// Always a user
+type AssignableUser struct {
+	id    string
+	login string
+	name  string
+}
+
+func NewAssignableUser(id, login, name string) AssignableUser {
+	return AssignableUser{
+		id:    id,
+		login: login,
+		name:  name,
+	}
 }
 
 // DisplayName returns a formatted string that uses Login and Name to be displayed e.g. 'Login (Name)' or 'Login'
-func (ra RepoAssignee) DisplayName() string {
-	if ra.Name != "" {
-		return fmt.Sprintf("%s (%s)", ra.Login, ra.Name)
+func (u AssignableUser) DisplayName() string {
+	if u.name != "" {
+		return fmt.Sprintf("%s (%s)", u.login, u.name)
 	}
-	return ra.Login
+	return u.login
 }
 
+func (u AssignableUser) ID() string {
+	return u.id
+}
+
+func (u AssignableUser) Login() string {
+	return u.login
+}
+
+func (u AssignableUser) Name() string {
+	return u.name
+}
+
+func (u AssignableUser) sealedAssignableActor() {}
+
+type AssignableBot struct {
+	id    string
+	login string
+}
+
+func (b AssignableBot) DisplayName() string {
+	return b.Login()
+}
+
+func (b AssignableBot) ID() string {
+	return b.id
+}
+
+func (b AssignableBot) Login() string {
+	return b.login
+}
+
+func (b AssignableBot) Name() string {
+	return ""
+}
+
+func (b AssignableBot) sealedAssignableActor() {}
+
 // RepoAssignableUsers fetches all the assignable users for a repository
-func RepoAssignableUsers(client *Client, repo ghrepo.Interface) ([]RepoAssignee, error) {
+func RepoAssignableUsers(client *Client, repo ghrepo.Interface) ([]AssignableUser, error) {
 	type responseData struct {
 		Repository struct {
 			AssignableUsers struct {
-				Nodes    []RepoAssignee
+				Nodes []struct {
+					ID    string
+					Login string
+					Name  string
+				}
 				PageInfo struct {
 					HasNextPage bool
 					EndCursor   string
@@ -1161,7 +1279,7 @@ func RepoAssignableUsers(client *Client, repo ghrepo.Interface) ([]RepoAssignee,
 		"endCursor": (*githubv4.String)(nil),
 	}
 
-	var users []RepoAssignee
+	var users []AssignableUser
 	for {
 		var query responseData
 		err := client.Query(repo.RepoHost(), "RepositoryAssignableUsers", &query, variables)
@@ -1169,7 +1287,15 @@ func RepoAssignableUsers(client *Client, repo ghrepo.Interface) ([]RepoAssignee,
 			return nil, err
 		}
 
-		users = append(users, query.Repository.AssignableUsers.Nodes...)
+		for _, node := range query.Repository.AssignableUsers.Nodes {
+			user := AssignableUser{
+				id:    node.ID,
+				login: node.Login,
+				name:  node.Name,
+			}
+
+			users = append(users, user)
+		}
 		if !query.Repository.AssignableUsers.PageInfo.HasNextPage {
 			break
 		}
@@ -1179,6 +1305,76 @@ func RepoAssignableUsers(client *Client, repo ghrepo.Interface) ([]RepoAssignee,
 	return users, nil
 }
 
+// RepoAssignableActors fetches all the assignable actors for a repository on
+// GitHub hosts that support Actor assignees.
+func RepoAssignableActors(client *Client, repo ghrepo.Interface) ([]AssignableActor, error) {
+	type assignableUser struct {
+		ID       string
+		Login    string
+		Name     string
+		TypeName string `graphql:"__typename"`
+	}
+
+	type assignableBot struct {
+		ID       string
+		Login    string
+		TypeName string `graphql:"__typename"`
+	}
+
+	type responseData struct {
+		Repository struct {
+			SuggestedActors struct {
+				Nodes []struct {
+					User assignableUser `graphql:"... on User"`
+					Bot  assignableBot  `graphql:"... on Bot"`
+				}
+				PageInfo struct {
+					HasNextPage bool
+					EndCursor   string
+				}
+			} `graphql:"suggestedActors(first: 100, after: $endCursor, capabilities: CAN_BE_ASSIGNED)"`
+		} `graphql:"repository(owner: $owner, name: $name)"`
+	}
+
+	variables := map[string]interface{}{
+		"owner":     githubv4.String(repo.RepoOwner()),
+		"name":      githubv4.String(repo.RepoName()),
+		"endCursor": (*githubv4.String)(nil),
+	}
+
+	var actors []AssignableActor
+	for {
+		var query responseData
+		err := client.Query(repo.RepoHost(), "RepositoryAssignableActors", &query, variables)
+		if err != nil {
+			return nil, err
+		}
+
+		for _, node := range query.Repository.SuggestedActors.Nodes {
+			if node.User.TypeName == "User" {
+				actor := AssignableUser{
+					id:    node.User.ID,
+					login: node.User.Login,
+					name:  node.User.Name,
+				}
+				actors = append(actors, actor)
+			} else if node.Bot.TypeName == "Bot" {
+				actor := AssignableBot{
+					id:    node.Bot.ID,
+					login: node.Bot.Login,
+				}
+				actors = append(actors, actor)
+			}
+		}
+
+		if !query.Repository.SuggestedActors.PageInfo.HasNextPage {
+			break
+		}
+		variables["endCursor"] = githubv4.String(query.Repository.SuggestedActors.PageInfo.EndCursor)
+	}
+	return actors, nil
+}
+
 type RepoLabel struct {
 	ID   string
 	Name string
diff --git a/api/queries_repo_test.go b/api/queries_repo_test.go
index 01fc7a4c7..9040a0018 100644
--- a/api/queries_repo_test.go
+++ b/api/queries_repo_test.go
@@ -526,17 +526,17 @@ func Test_RepoMilestones(t *testing.T) {
 func TestDisplayName(t *testing.T) {
 	tests := []struct {
 		name     string
-		assignee RepoAssignee
+		assignee AssignableUser
 		want     string
 	}{
 		{
 			name:     "assignee with name",
-			assignee: RepoAssignee{"123", "octocat123", "Octavious Cath"},
+			assignee: AssignableUser{"123", "octocat123", "Octavious Cath"},
 			want:     "octocat123 (Octavious Cath)",
 		},
 		{
 			name:     "assignee without name",
-			assignee: RepoAssignee{"123", "octocat123", ""},
+			assignee: AssignableUser{"123", "octocat123", ""},
 			want:     "octocat123",
 		},
 	}
diff --git a/api/query_builder.go b/api/query_builder.go
index 47fb4c225..0ef44a347 100644
--- a/api/query_builder.go
+++ b/api/query_builder.go
@@ -366,6 +366,8 @@ func IssueGraphQL(fields []string) string {
 			q = append(q, `headRepository{id,name}`)
 		case "assignees":
 			q = append(q, `assignees(first:100){nodes{id,login,name},totalCount}`)
+		case "assignedActors":
+			q = append(q, `assignedActors(first: 10){edges{node{...on Actor{login}}},totalCount}`)
 		case "labels":
 			q = append(q, `labels(first:100){nodes{id,name,description,color},totalCount}`)
 		case "projectCards":
diff --git a/internal/featuredetection/feature_detection.go b/internal/featuredetection/feature_detection.go
index fba317f58..a2f34a60b 100644
--- a/internal/featuredetection/feature_detection.go
+++ b/internal/featuredetection/feature_detection.go
@@ -18,11 +18,13 @@ type Detector interface {
 }
 
 type IssueFeatures struct {
-	StateReason bool
+	StateReason       bool
+	ActorIsAssignable bool
 }
 
 var allIssueFeatures = IssueFeatures{
-	StateReason: true,
+	StateReason:       true,
+	ActorIsAssignable: true,
 }
 
 type PullRequestFeatures struct {
@@ -70,7 +72,8 @@ func (d *detector) IssueFeatures() (IssueFeatures, error) {
 	}
 
 	features := IssueFeatures{
-		StateReason: false,
+		StateReason:       false,
+		ActorIsAssignable: false, // replaceActorsForAssignable GraphQL mutation unavailable on GHES
 	}
 
 	var featureDetection struct {
diff --git a/internal/featuredetection/feature_detection_test.go b/internal/featuredetection/feature_detection_test.go
index f1152da2c..2c7d19071 100644
--- a/internal/featuredetection/feature_detection_test.go
+++ b/internal/featuredetection/feature_detection_test.go
@@ -23,7 +23,8 @@ func TestIssueFeatures(t *testing.T) {
 			name:     "github.com",
 			hostname: "github.com",
 			wantFeatures: IssueFeatures{
-				StateReason: true,
+				StateReason:       true,
+				ActorIsAssignable: true,
 			},
 			wantErr: false,
 		},
@@ -31,7 +32,8 @@ func TestIssueFeatures(t *testing.T) {
 			name:     "ghec data residency (ghe.com)",
 			hostname: "stampname.ghe.com",
 			wantFeatures: IssueFeatures{
-				StateReason: true,
+				StateReason:       true,
+				ActorIsAssignable: true,
 			},
 			wantErr: false,
 		},
@@ -42,7 +44,8 @@ func TestIssueFeatures(t *testing.T) {
 				`query Issue_fields\b`: `{"data": {}}`,
 			},
 			wantFeatures: IssueFeatures{
-				StateReason: false,
+				StateReason:       false,
+				ActorIsAssignable: false,
 			},
 			wantErr: false,
 		},
diff --git a/pkg/cmd/issue/edit/edit.go b/pkg/cmd/issue/edit/edit.go
index 8386cbcfa..5cb789543 100644
--- a/pkg/cmd/issue/edit/edit.go
+++ b/pkg/cmd/issue/edit/edit.go
@@ -197,9 +197,24 @@ func editRun(opts *EditOptions) error {
 		}
 	}
 
+	if opts.Detector == nil {
+		cachedClient := api.NewCachedHTTPClient(httpClient, time.Hour*24)
+		opts.Detector = fd.NewDetector(cachedClient, baseRepo.RepoHost())
+	}
+
+	issueFeatures, err := opts.Detector.IssueFeatures()
+	if err != nil {
+		return err
+	}
+
 	lookupFields := []string{"id", "number", "title", "body", "url"}
 	if editable.Assignees.Edited {
-		lookupFields = append(lookupFields, "assignees")
+		if issueFeatures.ActorIsAssignable {
+			editable.Assignees.ActorAssignees = true
+			lookupFields = append(lookupFields, "assignedActors")
+		} else {
+			lookupFields = append(lookupFields, "assignees")
+		}
 	}
 	if editable.Labels.Edited {
 		lookupFields = append(lookupFields, "labels")
@@ -207,11 +222,6 @@ func editRun(opts *EditOptions) error {
 	if editable.Projects.Edited {
 		// TODO projectsV1Deprecation
 		// Remove this section as we should no longer add projectCards
-		if opts.Detector == nil {
-			cachedClient := api.NewCachedHTTPClient(httpClient, time.Hour*24)
-			opts.Detector = fd.NewDetector(cachedClient, baseRepo.RepoHost())
-		}
-
 		projectsV1Support := opts.Detector.ProjectsV1()
 		if projectsV1Support == gh.ProjectsV1Supported {
 			lookupFields = append(lookupFields, "projectCards")
@@ -254,7 +264,13 @@ func editRun(opts *EditOptions) error {
 
 		editable.Title.Default = issue.Title
 		editable.Body.Default = issue.Body
-		editable.Assignees.Default = issue.Assignees.Logins()
+		// We use Actors as the default assignees if Actors are assignable
+		// on this GitHub host.
+		if editable.Assignees.ActorAssignees {
+			editable.Assignees.Default = issue.AssignedActors.Logins()
+		} else {
+			editable.Assignees.Default = issue.Assignees.Logins()
+		}
 		editable.Labels.Default = issue.Labels.Names()
 		editable.Projects.Default = append(issue.ProjectCards.ProjectNames(), issue.ProjectItems.ProjectTitles()...)
 		projectItems := map[string]string{}
diff --git a/pkg/cmd/issue/edit/edit_test.go b/pkg/cmd/issue/edit/edit_test.go
index c9aa4c409..0df6d5e9f 100644
--- a/pkg/cmd/issue/edit/edit_test.go
+++ b/pkg/cmd/issue/edit/edit_test.go
@@ -118,9 +118,11 @@ func TestNewCmdEdit(t *testing.T) {
 			output: EditOptions{
 				IssueNumbers: []int{23},
 				Editable: prShared.Editable{
-					Assignees: prShared.EditableSlice{
-						Add:    []string{"monalisa", "hubot"},
-						Edited: true,
+					Assignees: prShared.EditableAssignees{
+						EditableSlice: prShared.EditableSlice{
+							Add:    []string{"monalisa", "hubot"},
+							Edited: true,
+						},
 					},
 				},
 			},
@@ -132,9 +134,11 @@ func TestNewCmdEdit(t *testing.T) {
 			output: EditOptions{
 				IssueNumbers: []int{23},
 				Editable: prShared.Editable{
-					Assignees: prShared.EditableSlice{
-						Remove: []string{"monalisa", "hubot"},
-						Edited: true,
+					Assignees: prShared.EditableAssignees{
+						EditableSlice: prShared.EditableSlice{
+							Remove: []string{"monalisa", "hubot"},
+							Edited: true,
+						},
 					},
 				},
 			},
@@ -354,10 +358,12 @@ func Test_editRun(t *testing.T) {
 						Value:  "new body",
 						Edited: true,
 					},
-					Assignees: prShared.EditableSlice{
-						Add:    []string{"monalisa", "hubot"},
-						Remove: []string{"octocat"},
-						Edited: true,
+					Assignees: prShared.EditableAssignees{
+						EditableSlice: prShared.EditableSlice{
+							Add:    []string{"monalisa", "hubot"},
+							Remove: []string{"octocat"},
+							Edited: true,
+						},
 					},
 					Labels: prShared.EditableSlice{
 						Add:    []string{"feature", "TODO", "bug"},
@@ -388,6 +394,7 @@ func Test_editRun(t *testing.T) {
 				mockIssueProjectItemsGet(t, reg)
 				mockRepoMetadata(t, reg)
 				mockIssueUpdate(t, reg)
+				mockIssueUpdateActorAssignees(t, reg)
 				mockIssueUpdateLabels(t, reg)
 				mockProjectV2ItemUpdate(t, reg)
 			},
@@ -399,10 +406,12 @@ func Test_editRun(t *testing.T) {
 				IssueNumbers: []int{456, 123},
 				Interactive:  false,
 				Editable: prShared.Editable{
-					Assignees: prShared.EditableSlice{
-						Add:    []string{"monalisa", "hubot"},
-						Remove: []string{"octocat"},
-						Edited: true,
+					Assignees: prShared.EditableAssignees{
+						EditableSlice: prShared.EditableSlice{
+							Add:    []string{"monalisa", "hubot"},
+							Remove: []string{"octocat"},
+							Edited: true,
+						},
 					},
 					Labels: prShared.EditableSlice{
 						Add:    []string{"feature", "TODO", "bug"},
@@ -433,6 +442,8 @@ func Test_editRun(t *testing.T) {
 				mockIssueProjectItemsGet(t, reg)
 				mockIssueUpdate(t, reg)
 				mockIssueUpdate(t, reg)
+				mockIssueUpdateActorAssignees(t, reg)
+				mockIssueUpdateActorAssignees(t, reg)
 				mockIssueUpdateLabels(t, reg)
 				mockIssueUpdateLabels(t, reg)
 				mockProjectV2ItemUpdate(t, reg)
@@ -449,10 +460,12 @@ func Test_editRun(t *testing.T) {
 				IssueNumbers: []int{123, 9999},
 				Interactive:  false,
 				Editable: prShared.Editable{
-					Assignees: prShared.EditableSlice{
-						Add:    []string{"monalisa", "hubot"},
-						Remove: []string{"octocat"},
-						Edited: true,
+					Assignees: prShared.EditableAssignees{
+						EditableSlice: prShared.EditableSlice{
+							Add:    []string{"monalisa", "hubot"},
+							Remove: []string{"octocat"},
+							Edited: true,
+						},
 					},
 					Labels: prShared.EditableSlice{
 						Add:    []string{"feature", "TODO", "bug"},
@@ -494,10 +507,12 @@ func Test_editRun(t *testing.T) {
 				IssueNumbers: []int{123, 456},
 				Interactive:  false,
 				Editable: prShared.Editable{
-					Assignees: prShared.EditableSlice{
-						Add:    []string{"monalisa", "hubot"},
-						Remove: []string{"octocat"},
-						Edited: true,
+					Assignees: prShared.EditableAssignees{
+						EditableSlice: prShared.EditableSlice{
+							Add:    []string{"monalisa", "hubot"},
+							Remove: []string{"octocat"},
+							Edited: true,
+						},
 					},
 					Milestone: prShared.EditableString{
 						Value:  "GA",
@@ -509,14 +524,14 @@ func Test_editRun(t *testing.T) {
 			httpStubs: func(t *testing.T, reg *httpmock.Registry) {
 				// Should only be one fetch of metadata.
 				reg.Register(
-					httpmock.GraphQL(`query RepositoryAssignableUsers\b`),
+					httpmock.GraphQL(`query RepositoryAssignableActors\b`),
 					httpmock.StringResponse(`
-					{ "data": { "repository": { "assignableUsers": {
+					{ "data": { "repository": { "suggestedActors": {
 						"nodes": [
-							{ "login": "hubot", "id": "HUBOTID" },
-							{ "login": "MonaLisa", "id": "MONAID" }
+							{ "login": "hubot", "id": "HUBOTID", "__typename": "Bot" },
+							{ "login": "MonaLisa", "id": "MONAID", "__typename": "User" }
 						],
-						"pageInfo": { "hasNextPage": false }
+						"pageInfo": { "hasNextPage": false, "endCursor": "Mg" }
 					} } } }
 					`))
 				reg.Register(
@@ -534,6 +549,14 @@ func Test_editRun(t *testing.T) {
 				mockIssueNumberGet(t, reg, 123)
 				mockIssueNumberGet(t, reg, 456)
 				// Updating 123 should succeed.
+				reg.Register(
+					httpmock.GraphQLMutationMatcher(`mutation ReplaceActorsForAssignable\b`, func(m map[string]interface{}) bool {
+						return m["assignableId"] == "123"
+					}),
+					httpmock.GraphQLMutation(`
+					{ "data": { "replaceActorsForAssignable": { "__typename": "" } } }`,
+						func(inputs map[string]interface{}) {}),
+				)
 				reg.Register(
 					httpmock.GraphQLMutationMatcher(`mutation IssueUpdate\b`, func(m map[string]interface{}) bool {
 						return m["id"] == "123"
@@ -544,8 +567,8 @@ func Test_editRun(t *testing.T) {
 				)
 				// Updating 456 should fail.
 				reg.Register(
-					httpmock.GraphQLMutationMatcher(`mutation IssueUpdate\b`, func(m map[string]interface{}) bool {
-						return m["id"] == "456"
+					httpmock.GraphQLMutationMatcher(`mutation ReplaceActorsForAssignable\b`, func(m map[string]interface{}) bool {
+						return m["assignableId"] == "456"
 					}),
 					httpmock.GraphQLMutation(`
 							{ "errors": [ { "message": "test error" } ] }`,
@@ -591,6 +614,7 @@ func Test_editRun(t *testing.T) {
 				mockIssueProjectItemsGet(t, reg)
 				mockRepoMetadata(t, reg)
 				mockIssueUpdate(t, reg)
+				mockIssueUpdateActorAssignees(t, reg)
 				mockIssueUpdateLabels(t, reg)
 				mockProjectV2ItemUpdate(t, reg)
 			},
@@ -670,16 +694,17 @@ func mockIssueProjectItemsGet(_ *testing.T, reg *httpmock.Registry) {
 
 func mockRepoMetadata(_ *testing.T, reg *httpmock.Registry) {
 	reg.Register(
-		httpmock.GraphQL(`query RepositoryAssignableUsers\b`),
+		httpmock.GraphQL(`query RepositoryAssignableActors\b`),
 		httpmock.StringResponse(`
-		{ "data": { "repository": { "assignableUsers": {
+		{ "data": { "repository": { "suggestedActors": {
 			"nodes": [
-				{ "login": "hubot", "id": "HUBOTID" },
-				{ "login": "MonaLisa", "id": "MONAID" }
+				{ "login": "hubot", "id": "HUBOTID", "__typename": "Bot" },
+				{ "login": "MonaLisa", "id": "MONAID", "__typename": "User" }
 			],
 			"pageInfo": { "hasNextPage": false }
 		} } } }
 		`))
+
 	reg.Register(
 		httpmock.GraphQL(`query RepositoryLabelList\b`),
 		httpmock.StringResponse(`
@@ -767,6 +792,15 @@ func mockIssueUpdate(t *testing.T, reg *httpmock.Registry) {
 	)
 }
 
+func mockIssueUpdateActorAssignees(t *testing.T, reg *httpmock.Registry) {
+	reg.Register(
+		httpmock.GraphQL(`mutation ReplaceActorsForAssignable\b`),
+		httpmock.GraphQLMutation(`
+		{ "data": { "replaceActorsForAssignable": { "__typename": "" } } }`,
+			func(inputs map[string]interface{}) {}),
+	)
+}
+
 func mockIssueUpdateLabels(t *testing.T, reg *httpmock.Registry) {
 	reg.Register(
 		httpmock.GraphQL(`mutation LabelAdd\b`),
@@ -791,6 +825,85 @@ func mockProjectV2ItemUpdate(t *testing.T, reg *httpmock.Registry) {
 	)
 }
 
+func TestActorIsAssignable(t *testing.T) {
+	t.Run("when actors are assignable, query includes assignedActors", func(t *testing.T) {
+		ios, _, _, _ := iostreams.Test()
+
+		reg := &httpmock.Registry{}
+		reg.Register(
+			httpmock.GraphQL(`assignedActors`),
+			// Simulate a GraphQL error to early exit the test.
+			httpmock.StatusStringResponse(500, ""),
+		)
+
+		_, cmdTeardown := run.Stub()
+		defer cmdTeardown(t)
+
+		// Ignore the error because we don't care.
+		_ = editRun(&EditOptions{
+			IO: ios,
+			HttpClient: func() (*http.Client, error) {
+				return &http.Client{Transport: reg}, nil
+			},
+			BaseRepo: func() (ghrepo.Interface, error) {
+				return ghrepo.New("OWNER", "REPO"), nil
+			},
+			Detector:     &fd.EnabledDetectorMock{},
+			IssueNumbers: []int{123},
+			Editable: prShared.Editable{
+				Assignees: prShared.EditableAssignees{
+					EditableSlice: prShared.EditableSlice{
+						Add:    []string{"monalisa", "octocat"},
+						Edited: true,
+					},
+				},
+			},
+		})
+
+		reg.Verify(t)
+	})
+
+	t.Run("when actors are not assignable, query includes assignees instead", func(t *testing.T) {
+		ios, _, _, _ := iostreams.Test()
+
+		reg := &httpmock.Registry{}
+		// This test should NOT include assignedActors in the query
+		reg.Exclude(t, httpmock.GraphQL(`assignedActors`))
+		// It should include the regular assignees field
+		reg.Register(
+			httpmock.GraphQL(`assignees`),
+			// Simulate a GraphQL error to early exit the test.
+			httpmock.StatusStringResponse(500, ""),
+		)
+
+		_, cmdTeardown := run.Stub()
+		defer cmdTeardown(t)
+
+		// Ignore the error because we're not really interested in it.
+		_ = editRun(&EditOptions{
+			IO: ios,
+			HttpClient: func() (*http.Client, error) {
+				return &http.Client{Transport: reg}, nil
+			},
+			BaseRepo: func() (ghrepo.Interface, error) {
+				return ghrepo.New("OWNER", "REPO"), nil
+			},
+			Detector:     &fd.DisabledDetectorMock{},
+			IssueNumbers: []int{123},
+			Editable: prShared.Editable{
+				Assignees: prShared.EditableAssignees{
+					EditableSlice: prShared.EditableSlice{
+						Add:    []string{"monalisa", "octocat"},
+						Edited: true,
+					},
+				},
+			},
+		})
+
+		reg.Verify(t)
+	})
+}
+
 // TODO projectsV1Deprecation
 // Remove this test.
 func TestProjectsV1Deprecation(t *testing.T) {
diff --git a/pkg/cmd/pr/edit/edit_test.go b/pkg/cmd/pr/edit/edit_test.go
index b09ee104e..4501626e7 100644
--- a/pkg/cmd/pr/edit/edit_test.go
+++ b/pkg/cmd/pr/edit/edit_test.go
@@ -166,9 +166,11 @@ func TestNewCmdEdit(t *testing.T) {
 			output: EditOptions{
 				SelectorArg: "23",
 				Editable: shared.Editable{
-					Assignees: shared.EditableSlice{
-						Add:    []string{"monalisa", "hubot"},
-						Edited: true,
+					Assignees: shared.EditableAssignees{
+						EditableSlice: shared.EditableSlice{
+							Add:    []string{"monalisa", "hubot"},
+							Edited: true,
+						},
 					},
 				},
 			},
@@ -180,9 +182,11 @@ func TestNewCmdEdit(t *testing.T) {
 			output: EditOptions{
 				SelectorArg: "23",
 				Editable: shared.Editable{
-					Assignees: shared.EditableSlice{
-						Remove: []string{"monalisa", "hubot"},
-						Edited: true,
+					Assignees: shared.EditableAssignees{
+						EditableSlice: shared.EditableSlice{
+							Remove: []string{"monalisa", "hubot"},
+							Edited: true,
+						},
 					},
 				},
 			},
@@ -360,10 +364,12 @@ func Test_editRun(t *testing.T) {
 						Remove: []string{"dependabot"},
 						Edited: true,
 					},
-					Assignees: shared.EditableSlice{
-						Add:    []string{"monalisa", "hubot"},
-						Remove: []string{"octocat"},
-						Edited: true,
+					Assignees: shared.EditableAssignees{
+						EditableSlice: shared.EditableSlice{
+							Add:    []string{"monalisa", "hubot"},
+							Remove: []string{"octocat"},
+							Edited: true,
+						},
 					},
 					Labels: shared.EditableSlice{
 						Add:    []string{"feature", "TODO", "bug"},
@@ -414,10 +420,12 @@ func Test_editRun(t *testing.T) {
 						Value:  "base-branch-name",
 						Edited: true,
 					},
-					Assignees: shared.EditableSlice{
-						Add:    []string{"monalisa", "hubot"},
-						Remove: []string{"octocat"},
-						Edited: true,
+					Assignees: shared.EditableAssignees{
+						EditableSlice: shared.EditableSlice{
+							Add:    []string{"monalisa", "hubot"},
+							Remove: []string{"octocat"},
+							Edited: true,
+						},
 					},
 					Labels: shared.EditableSlice{
 						Add:    []string{"feature", "TODO", "bug"},
diff --git a/pkg/cmd/pr/shared/completion.go b/pkg/cmd/pr/shared/completion.go
index e07abc5a7..c1296be71 100644
--- a/pkg/cmd/pr/shared/completion.go
+++ b/pkg/cmd/pr/shared/completion.go
@@ -21,13 +21,13 @@ func RequestableReviewersForCompletion(httpClient *http.Client, repo ghrepo.Inte
 
 	results := []string{}
 	for _, user := range metadata.AssignableUsers {
-		if strings.EqualFold(user.Login, metadata.CurrentLogin) {
+		if strings.EqualFold(user.Login(), metadata.CurrentLogin) {
 			continue
 		}
-		if user.Name != "" {
-			results = append(results, fmt.Sprintf("%s\t%s", user.Login, user.Name))
+		if user.Name() != "" {
+			results = append(results, fmt.Sprintf("%s\t%s", user.Login(), user.Name()))
 		} else {
-			results = append(results, user.Login)
+			results = append(results, user.Login())
 		}
 	}
 	for _, team := range metadata.Teams {
diff --git a/pkg/cmd/pr/shared/editable.go b/pkg/cmd/pr/shared/editable.go
index e73b3c294..d51405acd 100644
--- a/pkg/cmd/pr/shared/editable.go
+++ b/pkg/cmd/pr/shared/editable.go
@@ -14,7 +14,7 @@ type Editable struct {
 	Body      EditableString
 	Base      EditableString
 	Reviewers EditableSlice
-	Assignees EditableSlice
+	Assignees EditableAssignees
 	Labels    EditableSlice
 	Projects  EditableProjects
 	Milestone EditableString
@@ -38,6 +38,13 @@ type EditableSlice struct {
 	Allowed bool
 }
 
+// EditableAssignees is a special case of EditableSlice.
+// It contains a flag to indicate whether the assignees are actors or not.
+type EditableAssignees struct {
+	EditableSlice
+	ActorAssignees bool
+}
+
 // ProjectsV2 mutations require a mapping of an item ID to a project ID.
 // Keep that map along with standard EditableSlice data.
 type EditableProjects struct {
@@ -245,6 +252,13 @@ func (es *EditableSlice) clone() EditableSlice {
 	return cpy
 }
 
+func (ea *EditableAssignees) clone() EditableAssignees {
+	return EditableAssignees{
+		EditableSlice:  ea.EditableSlice.clone(),
+		ActorAssignees: ea.ActorAssignees,
+	}
+}
+
 func (ep *EditableProjects) clone() EditableProjects {
 	return EditableProjects{
 		EditableSlice: ep.EditableSlice.clone(),
@@ -378,12 +392,13 @@ func FieldsToEditSurvey(p EditPrompter, editable *Editable) error {
 
 func FetchOptions(client *api.Client, repo ghrepo.Interface, editable *Editable) error {
 	input := api.RepoMetadataInput{
-		Reviewers:  editable.Reviewers.Edited,
-		Assignees:  editable.Assignees.Edited,
-		Labels:     editable.Labels.Edited,
-		ProjectsV1: editable.Projects.Edited,
-		ProjectsV2: editable.Projects.Edited,
-		Milestones: editable.Milestone.Edited,
+		Reviewers:      editable.Reviewers.Edited,
+		Assignees:      editable.Assignees.Edited,
+		ActorAssignees: editable.Assignees.ActorAssignees,
+		Labels:         editable.Labels.Edited,
+		ProjectsV1:     editable.Projects.Edited,
+		ProjectsV2:     editable.Projects.Edited,
+		Milestones:     editable.Milestone.Edited,
 	}
 	metadata, err := api.RepoMetadata(client, repo, input)
 	if err != nil {
@@ -392,7 +407,11 @@ func FetchOptions(client *api.Client, repo ghrepo.Interface, editable *Editable)
 
 	var users []string
 	for _, u := range metadata.AssignableUsers {
-		users = append(users, u.Login)
+		users = append(users, u.Login())
+	}
+	var actors []string
+	for _, a := range metadata.AssignableActors {
+		actors = append(actors, a.Login())
 	}
 	var teams []string
 	for _, t := range metadata.Teams {
@@ -416,7 +435,11 @@ func FetchOptions(client *api.Client, repo ghrepo.Interface, editable *Editable)
 
 	editable.Metadata = *metadata
 	editable.Reviewers.Options = append(users, teams...)
-	editable.Assignees.Options = users
+	if editable.Assignees.ActorAssignees {
+		editable.Assignees.Options = actors
+	} else {
+		editable.Assignees.Options = users
+	}
 	editable.Labels.Options = labels
 	editable.Projects.Options = projects
 	editable.Milestone.Options = milestones
diff --git a/pkg/cmd/pr/shared/editable_http.go b/pkg/cmd/pr/shared/editable_http.go
index fcc30095a..8cd51c349 100644
--- a/pkg/cmd/pr/shared/editable_http.go
+++ b/pkg/cmd/pr/shared/editable_http.go
@@ -60,25 +60,78 @@ func UpdateIssue(httpClient *http.Client, repo ghrepo.Interface, id string, isPR
 
 	if dirtyExcludingLabels(options) {
 		wg.Go(func() error {
-			return replaceIssueFields(httpClient, repo, id, isPR, options)
+			// updateIssue mutation does not support Actors so assignment needs to
+			// be in a separate request when our assignees are Actors.
+			// Note: this is intentionally done synchronously with updating
+			// other issue fields to ensure consistency with how legacy
+			// user assignees are handled.
+			// https://github.com/cli/cli/pull/10960#discussion_r2086725348
+			if options.Assignees.Edited && options.Assignees.ActorAssignees {
+				apiClient := api.NewClientFromHTTP(httpClient)
+				assigneeIds, err := options.AssigneeIds(apiClient, repo)
+				if err != nil {
+					return err
+				}
+
+				err = replaceActorAssigneesForEditable(apiClient, repo, id, assigneeIds)
+				if err != nil {
+					return err
+				}
+			}
+			err := replaceIssueFields(httpClient, repo, id, isPR, options)
+			if err != nil {
+				return err
+			}
+
+			return nil
 		})
 	}
 
 	return wg.Wait()
 }
 
-func replaceIssueFields(httpClient *http.Client, repo ghrepo.Interface, id string, isPR bool, options Editable) error {
-	apiClient := api.NewClientFromHTTP(httpClient)
-	assigneeIds, err := options.AssigneeIds(apiClient, repo)
+func replaceActorAssigneesForEditable(apiClient *api.Client, repo ghrepo.Interface, id string, assigneeIds *[]string) error {
+	type ReplaceActorsForAssignableInput struct {
+		AssignableID githubv4.ID   `json:"assignableId"`
+		ActorIDs     []githubv4.ID `json:"actorIds"`
+	}
+
+	params := ReplaceActorsForAssignableInput{
+		AssignableID: githubv4.ID(id),
+		ActorIDs:     *ghIds(assigneeIds),
+	}
+
+	var mutation struct {
+		ReplaceActorsForAssignable struct {
+			TypeName string `graphql:"__typename"`
+		} `graphql:"replaceActorsForAssignable(input: $input)"`
+	}
+
+	variables := map[string]interface{}{"input": params}
+	err := apiClient.Mutate(repo.RepoHost(), "ReplaceActorsForAssignable", &mutation, variables)
 	if err != nil {
 		return err
 	}
 
+	return nil
+}
+
+func replaceIssueFields(httpClient *http.Client, repo ghrepo.Interface, id string, isPR bool, options Editable) error {
+	apiClient := api.NewClientFromHTTP(httpClient)
+
 	projectIds, err := options.ProjectIds()
 	if err != nil {
 		return err
 	}
 
+	var assigneeIds *[]string
+	if !options.Assignees.ActorAssignees {
+		assigneeIds, err = options.AssigneeIds(apiClient, repo)
+		if err != nil {
+			return err
+		}
+	}
+
 	milestoneId, err := options.MilestoneId()
 	if err != nil {
 		return err
diff --git a/pkg/cmd/pr/shared/survey.go b/pkg/cmd/pr/shared/survey.go
index bf4476ca1..b6c927a2d 100644
--- a/pkg/cmd/pr/shared/survey.go
+++ b/pkg/cmd/pr/shared/survey.go
@@ -192,7 +192,7 @@ func MetadataSurvey(p Prompt, io *iostreams.IOStreams, baseRepo ghrepo.Interface
 
 	var reviewers []string
 	for _, u := range metadataResult.AssignableUsers {
-		if u.Login != metadataResult.CurrentLogin {
+		if u.Login() != metadataResult.CurrentLogin {
 			reviewers = append(reviewers, u.DisplayName())
 		}
 	}
diff --git a/pkg/cmd/pr/shared/survey_test.go b/pkg/cmd/pr/shared/survey_test.go
index 6895b52ac..7097d0761 100644
--- a/pkg/cmd/pr/shared/survey_test.go
+++ b/pkg/cmd/pr/shared/survey_test.go
@@ -28,9 +28,9 @@ func TestMetadataSurvey_selectAll(t *testing.T) {
 
 	fetcher := &metadataFetcher{
 		metadataResult: &api.RepoMetadataResult{
-			AssignableUsers: []api.RepoAssignee{
-				{Login: "hubot"},
-				{Login: "monalisa"},
+			AssignableUsers: []api.AssignableUser{
+				api.NewAssignableUser("", "hubot", ""),
+				api.NewAssignableUser("", "monalisa", ""),
 			},
 			Labels: []api.RepoLabel{
 				{Name: "help wanted"},