Fuller has played television director Russell in Wayne's World; a mayoral aide in Ghostbusters II; the television executive and mastermind of the "Battle of the Tough Guys", Mr. Brell, in No Holds Barred; a real estate agent in Elvira: Mistress of the Dark; and NSC Director Robert Lindsey in the third season of Alias.

Fuller has also played real-life figures Werner Klemperer (in Paul Schrader's Auto Focus) and Karl Rove (on the TV satire That's My Bush!).

He also portrayed Pacific Bell Retirement Fund Executive Walter Ribbon in The Pursuit of Happyness.

Fuller has also appeared in many television shows, including Knight Rider, Timecop, Quantum Leap, L.A. Law, Murder, She Wrote, Ally McBeal, Felicity, Malcolm in the Middle, The West Wing, Boston Legal, Boston Public, House, Monk, Desperate Housewives, the live-action version of The Tick, Charmed, Carnivàle, My Name Is Earl, Ugly Betty, Glee, Drop Dead Diva and the pilot episode of NewsRadio.

He has had a recurring role as Woody the Coroner on Psych and another on Supernatural, portraying a malevolent angel called Zachariah.