As a young adult, he played a lead role in the 1957 Broadway and 1959 screen adaptations of Compulsion and in 1962, Stockwell played Edmund Tyrone in the film version of Long Day's Journey into Night. He appeared in supporting roles in such films as Paris, Texas (1984), To Live and Die in L.A. (1985), Blue Velvet (1986), Beverly Hills Cop II (1987), The Player (1992) and Air Force One (1997). He earned an Academy Award nomination for Best Supporting Actor for his performance in Married to the Mob (1988).
Stockwell was born in North Hollywood, California, but was raised in New York. He was the younger son of Elizabeth "Betty" Stockwell and Harry Stockwell, an actor and lyric baritone singer in New York productions of Carousel and Oklahoma as well as the voice of Prince Charming in Disney's film Snow White. His elder brother was television and film actor Guy Stockwell. His stepmother was Elizabeth Veronica Stockwell, an actress, comedian, singer and toe dancer in Burlesque and theatre in Northern America and New York..
In 1945, Stockwell appeared in a main character role (Donald Martin) in the musical movie Anchors Aweigh alongside Frank Sinatra and Gene Kelly. Some of his other child roles include that of Robert Shannon in The Green Years (1946); Gregory Peck's son in Gentleman's Agreement (1947); Nick Charles. Jr., in Song of the Thin Man (1947); as an orphaned runaway longing to go to sea in Deep Waters (1948); and as Lionel Barrymore's grandson and Richard Widmark's protégé in Down to the Sea in Ships (1949). He also starred in the lead role of The Boy with Green Hair in 1948, and in The Secret Garden in 1949. In 1950, he appeared in a lead role alongside Errol Flynn in Kim.
He resumed his acting career as an adult. In 1957, he starred as Judd Steiner in the Broadway adaptation of Compulsion, based on the Leopold and Loeb story; he played the same role in the 1959 film adaptation. In 1958, he joined Gloria Talbott and Dan Blocker as guest stars in the episode "Mercyday" of the NBC western series The Restless Gun, starring John Payne.
In 1960, he played coal miner's son Paul Morel in the British film Sons and Lovers, alongside Trevor Howard and Wendy Hiller. In 1961, he appeared in the premiere episode of ABC's Bus Stop series, which starred Marilyn Maxwell. In 1962, he appeared in an adaptation of Eugene O'Neill's play Long Day's Journey Into Night along with Katharine Hepburn, Ralph Richardson and Jason Robards. In 1964, Stockwell guest-starred in an episode of NBC's medical drama The Eleventh Hour.
In the mid-1960s, Stockwell dropped out of show business, becoming active in the Topanga Canyon hippie subculture as a close friend of artists George Herms and Wallace Berman, fellow child actor/"dropout" Russ Tamblyn and musician Neil Young.
Stockwell appeared in a 1969 episode of Bonanza as a down-and-out former Union soldier. He then appeared in two episodes of the mystery series Columbo. In 1973, he was the lead in a horror B-film, The Werewolf of Washington. During the mid-1970s, he worked as a real-estate broker and designed the distinctive cover of Young's American Stars 'n Bars (1976).
In 1984, he appeared in Wim Wenders' critically acclaimed film Paris, Texas, and in that same year, in David Lynch's film version of Dune as Wellington Yueh. The following year, he turned in a brief but significant role as attorney Bob Grimes in William Friedkin's To Live and Die in L.A.. In 1986, Stockwell made an appearance in another Lynch production, the neo-noir thriller Blue Velvet. In 1988, he was nominated for an Academy Award for Best Supporting Actor for his performance as Mafia boss Tony "the Tiger" Russo in the comedy Married to the Mob. He received a star on the Hollywood Walk of Fame on February 29, 1992 (Leap Day) following the success of Quantum Leap. In 1997 Stockwell co-starred with Harrison Ford and Glenn Close in the blockbuster suspense thriller Air Force One.
Along with Jack Lemmon and Marcello Mastroianni, Stockwell won the award for best actor at the Cannes Film Festival twice, for Compulsion and Long Day's Journey Into Night.
He joined the cast of the 2004 revival of Battlestar Galactica starting with its second-season finale, portraying what became the lead antagonist, Cylon John Cavil.
Dean Stockwell married Millie Perkins on April 15, 1960; they divorced on July 30, 1962. He married Joy Marchenko, a textiles expert who worked in Morocco, on December 15, 1981. They had two children: a son, Austin, born November 5, 1983, and a daughter, Sophia, born August 5, 1985.
Stockwell has been widely reported to be the godfather of actress Amber Tamblyn; in a 2009 interview with Parade, Tamblyn explained that "godfather" was "just a loose term" for Stockwell, Dennis Hopper and Neil Young, three famous friends of her father's, who were always around the house when she was growing up, and who were big influences on her life.
He is an accomplished artist who creates both digitally enhanced photographs and original collages in the style of Wallace Berman. During his time at the University of California, Berkeley, Stockwell immersed himself in music and wrote several small compositions. With Young, Stockwell co-wrote and co-directed the cult film Human Highway (1982). The title track from Young's 1970 album After the Gold Rush is based on an unproduced screenplay written by Stockwell and the reclusive Herb Bermann, a writer/actor best known for his work with Captain Beefheart.
Stockwell is an avid golfer and played golf during breaks in filming episodes of Quantum Leap. He is a martial artist, holding instructor rank in Modern Arnis.
He is an "avowed environmentalist", a characteristic which some of his onscreen characters have shared.
He campaigned for the Democrats in the 1992 US presidential election.