He is known for voicing Chucky in the Child's Play franchise (1988–present), portraying Gríma Wormtongue in The Lord of the Rings film series and his Oscar-nominated role as Billy Bibbit in One Flew Over the Cuckoo's Nest (1975).

Brad Dourif's other film roles include Wise Blood (1979), Ragtime (1981), Dune (1984), Blue Velvet (1986), Mississippi Burning (1988), The Exorcist III (1990), Critters 4 (1992), Alien Resurrection (1997), and the 2007 remake of Halloween and its sequel.

He also appeared in many television series, notably Deadwood (2004–2006, 2019), for which he received Primetime Emmy and Satellite Award nominations for his portrayal of Amos "Doc" Cochran.

Although he briefly considered becoming a flower arranger,[citation needed] he was eventually inspired to become an actor by his mother's participation as an actress in a community theater called Give Me Shelter.

"[7] Dourif attended Marshall University for a time, before quitting college and moving to New York City to study acting on the advice of actress Conchata Ferrell.

During the early 1970s, Dourif appeared in a number of plays, off-Broadway and at Woodstock, New York, including The Ghost Sonata, The Doctor in Spite of Himself, and When You Comin' Back, Red Ryder?, in which he was spotted by director Miloš Forman[8] who cast him in One Flew Over the Cuckoo's Nest (1975).

"[14] Dourif returned to New York, where he continued in theater and taught acting and directing classes at Columbia University until 1988 (Don Mancini[15] was among his students).

He continued with Eyes of Laura Mars (1978), John Huston's Wise Blood (1979),[16] Forman's Ragtime (1981), Marc Didden's Istanbul (1985) and David Lynch's Dune (1984) and Blue Velvet (1986).

He portrayed the Gemini Killer in The Exorcist III (1990) and appeared in Death Machine (1994), Sworn to Justice with Cynthia Rothrock and Alien Resurrection (1997).

Dourif later won acclaim as Doc Cochran in Deadwood, receiving a 2004 Emmy Award nomination for Outstanding Supporting Actor in a Drama Series.