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Cain was born Dean George Tanaka in Mount Clemens, Michigan, to actress Sharon Thomas and half-Japanese U.S. Army serviceman Roger Tanaka; he is one-quarter Japanese. His parents divorced before he was born. His mother later married film director Christopher Cain, and the family moved to Malibu, California. Christopher Cain adopted Dean and his brother, musician Roger Cain. The couple later had a daughter, Dean's half-sister, actress Krisinda Cain who also attended Santa Monica High.

At Santa Monica High School, Cain excelled in sports. He played on the baseball team, and Chad and Rob Lowe and Charlie Sheenówho played on the baseball teamówere among his classmates. When Cain graduated high school in 1984, he turned down 17 athletic scholarships to attend Princeton University, where he went on to be captain of the volleyball team and play free safety (Defensive Back) on the football team, where he had 12 interceptions in a single season, in addition to joining the Zeta Psi fraternity and the Cap & Gown eating club. He also dated actress Brooke Shields, who was one year ahead of him at the university. Cain graduated from Princeton in 1988 with a BA 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, an NFL football team, but a knee injury during training camp 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 television series Lois & Clark: The New Adventures of Superman, which ran until 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 Billions (2004). In 2004, he portrayed Scott Peterson in the fact-based made for television movie The Perfect Husband: The Laci Peterson Story. He has also appeared in a recurring role as Casey Manning in the television series Las Vegas. Recently, Cain guest-starred in a seventh season episode of Smallville as the immortal Dr. Curtis Knox.