Dourif began the 80s with a supporting role in Michael Cimino's notorious "Heaven's Gate" (1980), but had better luck reteaming with Milos Forman as the Evelyn Nesbitt-obsessed character (simply known as Younger Brother) in "Ragtime" (1981). The actor played featured roles in two David Lynch films, the overblown "Dune" (1984) and the highly praised "Blue Velvet" (1985). Under Tom Holland direction , Dourif played a nasty drug dealer in "Fatal Beauty" (1987) and developed a cult following as psycho Charles Lee Ray, whose spirit possesses a doll named Chucky, in Holland's "Child's Play" (1988). For the inevitable sequels ("Child's Play 2" 1990, "Child's Play 3" 1991 and "Bride of Chucky" 1998), Dourif provided the chilling voice of the demonic. The performer also offered a chilling turn as the villainously abusive Detective Pell in "Mississippi Burning" (1988) and was shown to good effect as a mental patient in "William Peter Blatty's The Exorcist III" (1990).

For much of the 90s, Dourif was trapped playing his patented oddballs and psychos in genre fare (e.g., "Critters 4" 1992), parts he has readily admitted he accepted to pay the bills. On occasion, there would be an interesting role, like the TV executive seduced by visual reality in "Wild Palms" (ABC, 1993), his memorable guest spot as a death row inmate claiming psychic powers in a 1994 episode of Fox's "The X-Files", and the 1996 recurring role of the crew member aiding in saving the titular spaceship from aliens in "Star Trek: Voyager" (UPN).

Dourif kicked off the new millennium playing a regular role as a local townsman in the PAX-TV prequel "Ponderosa" (2001). But perhaps his biggest chance came when he accepted the part of the spy Grima Wormtongue in Peter Jackson's anticipated tripartite adaptation of J.R.R. Tolkein's "The Lord of the Rings" (filmed 1999-2000) which opened over three years: "The Fellowship of the Ring" (2001), "The Two Towers" (2002) and "The Return of the King" (2003). Dourif first appeared in the second instalment, bringing characteristic oddball menace to his role. He was next nominated for an Emmy as best supporting actor in a TV drama for his impressive turn as Doc Cochran in HBO's hard-as-nails Western series "Deadwood" (2004- ).