Alan Ruck was born in Cleveland, Ohio, to a schoolteacher mother and a father who worked for a pharmaceutical company.^[1] He attended Parma Senior High School in Parma, Ohio, and graduated from the University of Illinois with a B.F.A. in drama in 1979.^[2] He recalled:

After school, I went up to Chicago, because I didn't really know anybody in New York or Los Angeles, and I knew people who were doing plays in Chicago. So I went up there, and I knocked around a little bit. And I guess about a year after I was out of school, I got my first job.

Ruck's first film role was in the 1983 drama film Bad Boys, in which he played Carl Brennan, Sean Penn's friend in the film. The same year, he played Roger Jackson in Class.

Ruck made his Broadway debut in 1985 in Neil Simon's Biloxi Blues with Matthew Broderick. He was soon a stage actor at theaters around the U.S., including the Wisdom Bridge Theatre in Chicago.

Ruck played Cameron Frye in John Hughes' 1986 comedy Ferris Bueller's Day Off, as the title character's hypochondriac best friend, after Broderick encouraged him to audition for the role; their real-life friendship was reportedly a factor in Ruck being cast.^[3][2] One of his other film roles was in the 1987 film Three for the Road.

Ruck later appeared in the 1989 comedy film Three Fugitives. Following that, he played Hendry William French in Young Guns II, the 1990 sequel to Young Guns. He played Captain Jonathan Harriman of the USS Enterprise-B in the 1994 film Star Trek Generations, a role that he reprised, along with Generations co-star Walter Koenig and other Trek alumni, in the fan film Of Gods and Men.^[4] Alan played an annoying tourist named Doug Stephens on an ill-fated bus in the 1994 blockbuster Speed. Another supporting role was of the eccentric storm chaser Robert 'Rabbit' Nurick in the 1996 disaster film Twister.^[5]

From 1990 to 1991, Ruck starred as Chicago ad man Charlie Davis, in the ABC series Going Places. ABC canceled the series after one season. He appeared in the series Daddy's Girls in 1994, which was canceled after three episodes. From 1996 to 2002, Alan played Stuart Bondek in the sitcom Spin City alongside Michael J. Fox and later, Charlie Sheen. In 2005, he played Leo Bloom in the Broadway version of Mel Brooks' The Producers, a role also played by Broderick, his Ferris Bueller co-star.

Ruck was then cast in the pilot of the Tim Minear-created Fox Network series Drive, but did not appear in the series. He also starred in one episode of the Comedy Central sitcom Stella as Richard, a man looking for work. He later starred in the season two Scrubs episode "My Lucky Day" as a patient, and played reporter Steve Jacobson on the ESPN miniseries The Bronx Is Burning.

In 1998, Ruck guest-starred in the fifth episode of the HBO miniseries From the Earth to the Moon as the NASA engineer Tom Dolan.

In 2006, Ruck guest-starred in a single episode of Stargate Atlantis called "The Real World" and, in 2007, as unscrupulous property developer Albert Bunford in an episode of Medium.

In the 2007 comedy Kickin' It Old Skool, he appears as Dr. Frye, a possible connection to Cameron Frye; he even mentions still trying to pay off an old Ferrari, a reference to Cameron totaling his dad's Ferrari in Ferris Bueller's Day Off.

Ruck played the part of a ghost of a family man in the 2008 film Ghost Town, which starred Ricky Gervais. Ruck also had a small role in the 2008 M. Night Shyamalan film The Happening.

In 2009, he had a minor role as Frank in an episode of Cougar Town, who has problems with his marriage due to a crush he had long ago on Jules, played by Courteney Cox. He played the role of Dean Bowman in the college fraternity drama Greek. He appeared in a guest role as a manic geologist in an episode of Eureka. He played Mr. Cooverman in the film I Love You, Beth Cooper. In 2009, Ruck filmed the medical drama Extraordinary Measures^[6][7] in Portland, Oregon, with star Harrison Ford.

Ruck appeared as a bank robber in a season three episode of the USA Network series Psych, and as a lawyer in season five of the ABC series Boston Legal. He guest-starred as Martin, a magazine reporter, on an episode of Ruby & the Rockits entitled "We Are Family?"

In 2010, Ruck was cast as a lead character in the NBC mystery-drama, Persons Unknown. He guest-starred on the television show Fringe as a scientist turned criminal, in the NCIS: Los Angeles season two episode "Borderline", and guest-starred as ex-money laundering accountant turned dentist on an episode of Justified entitled "Long in the Tooth". He appeared in the Grey's Anatomy season five episode "In The Midnight Hour".

In 2012, Ruck was cast in the ABC Family series Bunheads as the husband to Sutton Foster's character, Michelle. In 2013, he appeared in NCIS, guest-starring in the season 11 episode, "Gut Check".

In autumn 2016, Ruck began a 10-episode run on The Exorcist as Henry Rance, the husband (who has suffered mild brain damage in a vaguely explained accident) of Angela Rance (Geena Davis), better known as the adult Regan MacNeil, the tortured girl (played by Linda Blair) who is possessed by a demon in the 1973 hit film The Exorcist.

From 2018 to 2023, Ruck played the role of Connor Roy, the eldest son of a media magnate, in the HBO series Succession. He was part of the cast's win for the Screen Actors Guild Award for Outstanding Performance by an Ensemble in a Drama Series in 2022 and 2024. In 2023, he received Golden Globe and Emmy nominations for his performance.^[8]

Ruck was married to actress Claudia Stefany from 1984 to 2005, with whom he has two children.^[9][10][11] Since 2008, he has been married to actress Mireille Enos, whom he met in 2005 while co-starring in the Broadway revival of Absurd Person Singular.^[10] They have two children.^[12]

On October 31, 2023, Ruck was involved in a car crash in Los Angeles. For unknown reasons, he lost control of his Rivian R1T, hit several vehicles, and crashed into the side of a pizza restaurant.^[13]