Born into a prominent acting family, Bridges appeared on the television series Sea Hunt (1958–1960) alongside his father, Lloyd, and brother, Beau.

He made his feature film debut in the drama Halls of Anger (1970), and starred in The Last Picture Show (1971), which earned him his first Academy Award nomination.

On television, he earned Primetime Emmy Award nominations for his performances in the HBO film A Dog Year (2009), and the Hulu series The Old Man (2022–2024).

At age 17 he toured with his father in a stage production of Anniversary Waltz, and then moved to New York City, where he studied acting at the Herbert Berghof Studio.

[18] In 1982, Bridges starred in one of his better-known roles in the science fiction film Tron, in which he played Kevin Flynn, a video game programmer.

[21] In 1984, he starred in the John Carpenter directed science fiction romance Starman playing an alien opposite Karen Allen.

[10] During this period he also performed in the neo-noir Against All Odds (1984) with James Woods and Rachel Ward,[22] the thrillers Jagged Edge (1985) opposite Glenn Close[23] and The Morning After (1986) with Jane Fonda,[24] and the crime comedy Nadine (1987) alongside Kim Basinger.

[28] The following year he starred in Terry Gilliam's fantasy comedy-drama The Fisher King (1991) opposite Robin Williams, Mercedes Ruehl and Amanda Plummer.

In the film he plays a misanthropic radio shock jock who befriends a homeless person on the quest to find love and the Holy Grail.

[30] In 1992 he produced and starred as a man released from prison in the Martin Bel directed drama American Heart earning the Independent Spirit Award for Best Male Lead.

"[32] In 1993 he starred in the Peter Weir directed drama Fearless (1993) alongside Isabella Rossellini, John Turturro, and Rosie Perez.

[38][39] In 1996 he acted in the Showtime television film Hidden in America alongside his brother Beau Bridges and Frances McDormand.

[40] The following year acted in Ridley Scott's survival drama White Squall and co-starred with Barbra Streisand in the romantic comedy The Mirror Has Two Faces.

[10] He played a fictional president of the United States in the political drama The Contender acting opposite Gary Oldman and Joan Allen.

[41] He portrayed businessman Charles S. Howard in the horse racing drama film Seabiscuit co-starring with Tobey Maguire and Chris Cooper.

Bridges also narrated the documentaries National Geographic's Lewis & Clark: Great Journey West (2002, IMAX), Discovery Channel's Raising the Mammoth (2000), and ABC's Heroes of Rock and Roll (1979).

[52] In 2009, he acted in the satirical comedy The Men Who Stare at Goats alongside George Clooney, Ewan McGregor, and Kevin Spacey.

[54] Bridges received his sixth Academy Award nomination for his role in True Grit, a collaboration with the Coen brothers in which he starred alongside Matt Damon, Josh Brolin, Barry Pepper, and Hailee Steinfeld.

[57] Bridges found himself at a party with Glassman and Ram Dass and their conversation led to discussing the parallels between "The Dude" from The Big Lebowski and Zen Buddhism.

"[59] The following year he produced and starred as the title role in dystopian drama The Giver and acted in the action fantasy film Seventh Son, which were both critically panned and the latter a box office flop.

The following year he narrated the documentary Dream Big: Engineering Our World (2015) and acted in the Taylor Sheridan directed neo-Western drama film Hell or High Water (2015) opposite Chris Pine and Ben Foster.

[63] In 2017, he acted in the romantic drama The Only Living Boy in New York with Callum Turner and Kate Beckinsale and in the spy action comedy Kingsman: The Golden Circle starring Taron Egerton and Colin Firth.

[64] In 2018 he acted in the neo-noir ensemble thriller Bad Times at the El Royale with Cynthia Erivo, Dakota Johnson, and Jon Hamm.

[73] Before his first lead role as an actor he already sold two songs to the acclaimed musician and composer Quincy Jones, who used his "Lost in Space" for the soundtrack of the 1970 film John and Mary and let Bridges contribute the vocals.

In 1982, he voiced the character of Prince Lír in the animated film The Last Unicorn, and in that role sang on two songs, including a duet with Mia Farrow.

In the film The Contender, in which he co-starred, Bridges recorded a version of Johnny Cash's standard "Ring of Fire" with Kim Carnes that played over the pivotal opening credits.

[78] In 2015, he sang on the album Strangers Again, performing a duet with Judy Collins of the song "Make Our Garden Grow" from Candide by Leonard Bernstein.

In 2020, Bridges partnered with Breedlove Guitars to release his signature Oregon Concerto Bourbon CE with "All In This Together" scrawled across the fretboard.

He began taking photographs on film sets during Starman at the suggestion of co-star Karen Allen in 1984, with his favorite camera, a Widelux F8 that his wife bought him.