A
- Adam Kaufman as Parker Abrams
- George Hertzberg as Adam
- Sarah Hagan as Amanda
- Jack Stehlin as Doctor Francis Angleman
- Andrew J. Ferchland as The Anointed One
B
- Larry Bagby III as Larry Blaisdell
C
- Nathan Fillion as Caleb
- Robia LaMorte as Jenny Calendar
- Dania Ramirez as Caridad
- Kristy Wu as Chao-Ahn
- Lalaine as Chloe
- James C. Leary as Clem
D
- Andy Umberger as D’Hoffryn
- Julie Benz as Darla
- Joel Grey as Doc
- Kevin Weisman as Dreg
- Juliet Landau as Drusilla
F
- Jack Plotnick as Deputy Mayor Allan Finch
- Ken Lerner as Principal Bob Flutie
G
- Leonard Roberts as Forrest Gates
- Clare Kramer as Glory
H
- Kali Rocha as Halfrek
- Fab Filippo as Scott Hope
J
- Troy T. Blendell as Jinx
K
- Mercedes McNab as Harmony Kendall
- Iyari Limon as Kennedy
L
- Eliza Dushku as Faith Lehane
- Danny Strong as Jonathan Levinson
M
- Elizabeth Anne Allen as Amy Madison
- Mark Metcalf as The Master
- Jason Hall as Devon MacLeish
- Eric Balfour as Jesse McNally
- Conor O’Farrell as Colonel McNamara
- Adam Busch as Warren Mears
- Bailey Chase as Graham Miller
- Clara Bryant as Molly
- Todd Duffey as Murk
N
- Dagney Kerr as Kathy Newman
- Azura Skye as Cassie Newton
P
- Sharon Ferguson as The Primitive
R
- Jeff Kober as Rack
- Robin Sachs as Ethan Rayne
- Indigo as Rona
S
- Megan Gray as Sandy
- Mary Wilcher as Shannon
- Amelinda Embry as Katrina Silber
- Armin Shimerman as Principal R. Snyder
- Julia Lee as Anne Steele
- Dean Butler as Hank Summers
- Kristine Sutherland as Joyce Summers
T
- Harris Yulin as Quentin Travers
- K. Todd Freeman as Mr. Trick
- Camedon Toy as The Turok-Han
V
W
- Lindsay Crouse as Professor Maggie Walsh
- Tom Lenk as Andrew Wells
- Ethan Erickson as Percy West
- Harry Groener as Mayor Richard Wilkins III
- Charlie Weber as Ben Wilkinson
- Phina Oruche as Olivia Williams
- Saverio Guerra as Willy
- April Wheedon-Washington / K.D. Aubert as Nikki Wood
- D.B. Woodside as Robin Wood
- Alexis Denisof as Wesley Wyndam-Pryce
Y
- Bianca Lawson as Kendra Young
The Watcher's Guide 