Slater was born Christian Michael Leonard Slater in New York City, the son of Mary Jo Slater, a casting executive, and Michael Hawkins (nee Thomas Knight Slater), an actor who is also known as Michael Gainsborough. Slater has a maternal half-brother, Ryan, who is also an actor.Slater attended the Dalton School, the Professional Children's School and the Fiorello H. LaGuardia High School of Music & Art and Performing Arts.

He has been erroneously thought to be related to Helen Slater. In addition to their shared professional surname, the myth is further fueled by their portrayal of sister and brother in The Legend of Billie Jean. Additionally, the DVD of Supergirl, featuring Helen Slater, included a critic's review which wrongly stated she is his sister.

Following a run on the ABC soap opera One Life to Live, he made his Broadway debut as the lisping Winthrop Paroo opposite Dick Van Dyke in the 1980 revival of The Music Man. Additional Broadway credits include Copperfield, Merlin, Macbeth, Side Man, and The Glass Menagerie. He made his big screen debut in 1985 in the film The Legend of Billie Jean. He had significant roles in the 1986 mystery film The Name of the Rose, the 1989 dark comedy Heathers, and the 1990 teen film Pump Up the Volume. His most notable roles from the '90s include the role of outlaws "Arkansas" Dave Rudabaugh in Young Guns II in 1990 and "Clarence Worley" in True Romance in 1993. He also voiced the character "John Watson" a.k.a. "Wonko the Sane" in BBC Radio 4's production of Hitchhiker's Guide to the Galaxy.

He was starring in NBC's My Own Worst Enemy, but it has been canceled due to low ratings.