Dean George Tanaka was born on July 31, 1966 in Mount Clemens, Michigan, the biological son of Roger Tanaka and actress Sharon Thomas. He is of French Canadian, Irish, Japanese, and Welsh descent. In 1969, Cain's mother married film director Christopher Cain, who adopted Dean and his brother, musician Roger Cain; the family moved to Malibu, California. They later had a daughter, actress Krisinda Cain.
Cain attended Santa Monica High School, where he excelled in sports. Among his schoolmates were Charlie Sheen, who played on the same baseball team as Cain when they were children, as well as Rob Lowe and his brother, Chad. He graduated from high school in 1984 and attended Princeton University, where he played football. He dated actress Brooke Shields while at the university. He graduated in 1988 with a Bachelor of Arts in history; his senior thesis was titled "The History and Development of the Functions of the Academy of Motion Picture Arts and Sciences".
Immediately after graduating, Cain signed on as a free agent with the Buffalo Bills, but a knee injury during training camp ended his football career prematurely. With little hope of returning to sports, he turned to screenwriting and then acting, shooting dozens of commercials including a volleyball-themed spot for Kellogg's Frosted Flakes and appearing on popular television shows like Grapevine, A Different World and Beverly Hills, 90210. In 1993, Cain took on his biggest role to date as Superman in the television series Lois & Clark: The New Adventures of Superman. At the height of its popularity, it would bring in an average of at least 15 million viewers per episode. The series ran for four seasons, ending in 1997.
In 1998, Cain started the Angry Dragon Entertainment production company, which produced the TBS Superstation television series Ripley's Believe It or Not!. He has also starred in several films, including The Broken Hearts Club (2000), Out of Time (2003) and Bailey's Billion$ (2004). In 2004, he portrayed Scott Peterson in the fact-based made-for-television movie The Perfect Husband: The Laci Peterson Story. He appeared in a recurring role as Casey Manning in the television series Las Vegas. Cain made a return to the Superman franchise, with a special guest role in a season seven episode of Smallville as the immortal Dr. Curtis Knox, a character based upon the DC Comics villain Vandal Savage; and again in a recurring role on Supergirl, as the title character's foster father, Jeremiah Danvers. He is also the star of the VH1 hit series Hit the Floor as Pete Davenport, who is the new head coach of a fictional NBA team and has an illegitimate daughter who is a cheerleader for his NBA team. He was ranked No. 33 on VH1's 40 Hottest Hotties of the '90s.
Cain was also a contestant in an NBC celebrity reality competition series called Stars Earn Stripes. He won four out of six missions on the show, though he came in third in the finals. In 2012, he participated in Fox's dating game show The Choice.
In 2013, Cain hosted a reality show about Bigfoot called 10 Million Dollar Bigfoot Bounty, where he offered contestants $10 Million to prove the existence of Bigfoot.
Cain appeared in the mid-season premiere of Comic Book Men, appearing at Kevin Smith's Secret Stash where the crew was celebrating 75 years of Superman, citing that Dean Cain helped people care about Superman again.
Cain appeared in the film God's Not Dead, in which he plays an arrogant businessman.
In 2016, Cain played a guest role on the Netflix original series Lady Dynamite as Graham the ex-fiance of Maria Bamford.
While the two were both attending Princeton University, Cain dated actress Brooke Shields for two years. In 1997, Cain became engaged to singer Mindy McCready. The couple broke up the following year. He has a son named Christopher Dean Cain (born June 11, 2000) with ex-girlfriend and Playboy Playmate Samantha Torres. Cain named his son after his adoptive father, film director Christopher Cain.
Cain supported Republican candidate Rick Perry for President in the 2012 election. In 2016, he endorsed Donald Trump.