Born Dean George Tanaka, in Mount Clemens, Michigan to actress Sharon Thomas and U.S. Army serviceman Roger Tanaka. His parents divorced before he was born, but his mother later married film director Chris Cain and moved to Malibu, California.

At Santa Monica High School, Cain excelled in sports. When he graduated in 1984, he turned down 17 athletic scholarships to attend Princeton University, where he went on to captain the volleyball team and play free safety on the football team (setting the NCAA record for the most interceptions in a single season), in addition to joining the Zeta Psi fraternity. He was also rumored to have dated actress Brooke Shields who was one year ahead of him at the university. Cain graduated from Princeton in 1988 with an B.A. in history. The title of his senior thesis was 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, a NFL football team, but a knee injury during training ended his football career before it began. With little hope of returning to sports, he turned to screenwriting and then acting, shooting dozens of commercials and appearing on popular television shows like Grapevine, A Different World and Beverly Hills 90210. In 1993, Cain took on the role of Superman in the new television series Lois and Clark: The New Adventures of Superman, which ran until 1997.

In 1998, Cain started the Angry Dragon Entertainment production company, which produces the new 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 Billions (2004). In 2004 he portrayed Scott Peterson in the fact-based made for television movie The Perfect Husband: The Laci Peterson Story.

Dean Cain is a quarter Japanese, French-Canadian, Irish and Welsh and has a son, Christopher Dean Cain, with former girlfriend and Playboy model Samantha Torres.