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Ontkean began in Hollywood by guest starring in The Partridge Family in 1971, and he was a television guest player on such shows as Ironside and Longstreet, but his break was in the ABC series The Rookies (1972–1976), in which he played Officer Willie Gillis for the first two seasons. He was replaced by actor, Bruce Fairbairn in The Rookies. Ontkean's hockey skill played a large role in his landing the role of Ned Braden in Slap Shot (1977), as he performed all of his on-ice shots himself. In 1979, he appeared in the first episode of Tales of the Unexpected.
Other early movie roles included Necromancy (1972) with Orson Welles; Voices (1979) with Amy Irving; Willie & Phil (1980) with Margot Kidder; The Blood of Others (1984); Kids Don't Tell (1985) with JoBeth Williams; The Right of the People (1986); The Allnighter and Maid to Order (both 1987) (the latter with Ally Sheedy); Clara's Heart (1988) with Whoopi Goldberg, and Bye Bye Blues (1989).
Making Love (1982) is about a married man who discovers his homosexuality. Ontkean was not the director's first choice for the film: Arthur Hiller had previously approached Tom Berenger, Michael Douglas, Harrison Ford, William Hurt and Peter Strauss to play the lead, before finally approaching Ontkean. According to Hiller, the reaction of most actors was to tell him not to even consider them for the role. The film reunited Ontkean with Kate Jackson; the two had previously co-starred together in The Rookies. Many years later, Ontkean tried to prevent clips from the film from being included in The Celluloid Closet, a 1996 documentary about LGBT characters in film, but he was unsuccessful.
Ontkean appeared as Sheriff Harry S. Truman in David Lynch and Mark Frost's Twin Peaks (1990–1991). He filmed scenes for Twin Peaks: Fire Walk with Me but, like many others from the original TV series, his scenes were deleted from the final film.
Ontkean subsequently appeared in many film and television productions including In Defense of a Married Man (1990); In a Child's Name (1991) with Valerie Bertinelli; Legacy of Lies (1992); Rapture and Vendetta II: The New Mafia (both 1993); Swann: A Mystery and The Stepford Husbands (both 1996); Summer of the Monkeys and A Chance of Snow (both 1998; the latter again with JoBeth Williams); Bear with Me (2000), and Mrs. Ashboro's Cat (2003).
Ontkean had a recurring role on Fox's short-lived series North Shore in 2004, and also appeared in the 2008 comedy TV show Sophie.
He had a supporting role in the 2011 film The Descendants, which was his last role to date before he decided to retire from acting. The movie was filmed in Hawaii, where he lives.
Ontkean was approached to reprise his role as Sheriff Truman for the 2017 revival of Twin Peaks. At first, Ontkean was reportedly excited about returning to the role, and enlisted Twin Peaks authority Brad Dukes to help him find the jacket which his character once wore on the show. Dukes located a suitable replica, bought it and sent it to Ontkean. However, in 2015, Ontkean officially dropped out of the Twin Peaks revival, for reasons which were never made public. Dukes recalled: "We last spoke in August and he informed me he wasn’t going to Washington after all. I told him I was heartbroken to hear that. Aside from being heartbroken, I am puzzled. Twin Peaks is not Twin Peaks without Michael Ontkean as Sheriff Harry S. Truman."
Ontkean's role was replaced by Robert Forster, playing Sheriff Truman's brother Frank. Forster was initially David Lynch's first choice to play Harry Truman in 1990.