[2] Ontkean relocated to the United States to attend the University of New Hampshire on a hockey scholarship before pursuing a career in acting in the early 1970s.

In 1982, he had a starring role opposite Harry Hamlin and Kate Jackson in the drama Making Love, in which he portrayed a married man who comes to terms with his homosexuality.

Ontkean continued to appear in films, such as Clara's Heart (1988) and Postcards from the Edge (1990) before being cast as Sheriff Harry S. Truman on David Lynch's Twin Peaks (1990–1991).

[6] Ontkean began in Hollywood by guest starring in The Partridge Family in 1971, and had guest roles on such shows as Ironside and Longstreet, but his break was in the ABC series The Rookies (1972–1976),[2] in which he played Officer Willie Gillis for the first two seasons;[citation needed] he left the show and was succeeded by actor Bruce Fairbairn.

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).

[12] 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.

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.