Dreyfus’ career as an actor began early. At the age of 15, Dreyfus made his debut for the television production, ‘In Mama’s House’. Following this, he briefly attended San Fernando Valley State College, (now California State University), for a year.
During Vietnam War, Dreyfus worked as a clerk in a Los Angeles hospital. He returned to acting, making guest appearance in television shows such as ‘Peyton Place’, ‘Gidget’, ‘That Girl’, ‘Bewitched’ and ‘The Big Valley’.
Drefus made his debut on the big screen with a small, uncredited role in the 1967 film ‘The Graduate’. Next, he featured in ‘Valley of the Dolls’ (1967) wherein he had a small role yet again.
During the late 1960s and early 1970s, Dreyfus performed on stage on Broadway, Off-Broadway, repertory, and improvisational theatre. He shared the stage with Henry Fonda, Gloria Grahame, Ron Thompson, Strother Martin, Jane Alexander, Lewis J. Stadlen, Richard X. Slattery and Pepper Martin for the play ‘The Time of Your Life’.
In 1973, Dreyfus played a significant role in the flick, ‘American Graffiti’. The movie was a major hit and had him share the screen space with Harrison Ford and Ron Howard.
In 1974, Dreyfus f played the lead role in the Canadian film, ‘The Apprenticeship of Duddy Kravitz’. The film was positively received by the audience and the critics alike. Dreyfus acting talent was praised and appreciated.
Year 1975 was a prosperous year for Dreyfus in terms of career. He starred in the box office blockbuster, ‘Jaws’, directed by Steven Spielberg. The film was one of the top grossing films of the decade and established Dreyfus’ reputation as a star actor.
Dreyfus repeated his success story with Spielberg yet again in the 1977 flick, ‘Close Encounters of the Third Kind’. The film went on to become one of the biggest hits of the decade. Same year, he was seeing playing a romantic lead in ‘The Goodbye Girl’. Such was the finesse with which he played the role of a struggling actor in the film that he bagged the 1978 Academy Award for Best Actor. With this, he became the youngest actor to claim the award. His record stood for 25 years before it was broken by Adrian Brody in 2003.
Following ‘The Goodbye Girl’ success story, Dreyfus produced and starred in the movie ‘The Big Fix’ in 1978. It was around this time that Dreyfus’ addiction for cocaine began. For most of the early 1980s, he suffered from drug addiction. In 1982, he was arrested for possession of drugs. His films of this period were major duds at the box-office.
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Around mid-1980s, Dreyfus entered rehabilitation. He made his comeback with the 1986 Paul Mazursky's film, ‘Down and Out in Beverly Hills’, starring alongside Bette Midler and Nick Nolte. Same year, he capped the role of narrator Gordie LaChance in Rob Reiner’s ‘Stand By Me’, a coming-of-age comedy-drama adapted from Stephen King’s novella ‘The Body’.
In 1987, Dreyfus starred in the films, ‘Stakeout’, ‘Nuts’ and ‘Tin Men’. Following year, he once again united with director Paul Mazursky for the romantic comedy ‘Moon Over Parador’.
In the second innings of his career, Dreyfus established himself as an engaging lead actor. In 1989, he reunited with Steven Spielberg for the film, ‘Always’ co-starring with Holly Hunter. The film was a remake of ‘A Guy Named Joe’.
He started the decade of 1990s with the films, ‘Postcards from the Edge’ and Rosencrantz & Guildenstern Are Dead’. In 1991, he was a part of the ensemble cast in the rom-com, ‘Once Around’. Same year, he starred in Bill Murray’s popular comedy ‘What About Bob?’ In it, he played the role of a psychiatrist who goes crazy while treating his obsessive new patient. He ended the year with the film, ‘Prisoner of Honor’ which he produced and starred in.
In 1994, he was one of the participants of the historic Papal Concert commemorating the Shoah at the Vatican amidst Pope John Paul II, Rav Elio Toaf - chief rabbi of Rome, and Oscar Luigi Scalfaro - President of the Italian Republic. He recited Kaddish as part of a performance of Leonard Bernstein's Third Symphony with the Royal Philharmonic Orchestra under the baton of Gilbert Levine.
Year 1995 was a big year for Dreyfus in terms of career. He started the year with a supporting role in ‘The American President’ but ended it on a handsome note as Glenn Holland in ‘Mr. Holland's Opus’. His role of a determined and inspiring musical teacher to a deaf son earned him nomination for Best Actor in both Academy and Golden Globe Awards.
Beginning 2000, he appeared in several films, including ‘The Crew’, ‘The Old Man Who Read Love Stories’, ‘Who Is Cletis Tout?’ and ‘Silver City’.
He featured as one of the survivors in the 2006 film, ‘Poseidon’. In 2008, he played the character of U.S Vice President Dick Cheney in Oliver Stone's George W. Bush’s biopic ‘W’.
In 2010, he made a cameo appearance in ‘Piranha 3D’ as Matt Hooper. Same year, he also starred in the film, ‘RED’. In 2015, he was seen playing the role of George Hiller in the film, ‘Zipper’.
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In 2016, Dreyfus portrayed the role of Bernie Madoff in the miniseries ‘Madoff’ co-starring Blythe Danner.
In addition to films, theatre and television, Dreyfus made his presence felt in literary world too with his book, ‘The Two Georges’, which he co-authored with science-fiction writer Harry Turtledove.