Hall's acting career began in the theater. Off-Broadway, he appeared in Macbeth and Cymbeline at the New York Shakespeare Festival, and in Timon of Athens and Henry V at the New York Public Theater, The English Teachers at the Manhattan Class Company (MCC), and the controversial play Corpus Christi at the Manhattan Theatre Club. He also performed in the workshop production of what was then known as Sondheim's Wise Guys, which has metamorphosed into Bounce. He sang the role of Paris Singer; this character's songs and function in the play were transferred to the character Hollis Bessamer in the final version of the play. In Los Angeles, he appeared in Skylight at the Mark Taper Forum.

In 1999, director Sam Mendes cast Hall as the flamboyant Emcee in the revival of Cabaret, his first Broadway role. Mendes also directed the film American Beauty, written by Alan Ball, and he suggested Hall for the role of deeply closeted David Fisher when Ball began casting the TV drama Six Feet Under. "Everything I opened up for Cabaret," Hall reported in a 2004 interview, "I slammed shut for David."

Hall's work in the first season of Six Feet Under was recognized by a 2002 Emmy nomination for a Outstanding Lead Actor in a Drama Series and 2002 AFI Award nomination for Actor of the Year. In addition, he shared in the Screen Actors Guild nomination for best ensemble cast all five years that the show was in production, winning the award in 2003 and 2004.

In 2003, Hall toured as Billy Flynn in the musical Chicago. His only film credit is the 2003 thriller Paycheck, and he also appeared in the 2003 TV movie Bereft. In 2005 he returned to Off-Broadway theatre in the premiere of Noah Haidle's Mr. Marmalade, playing the title character, an emotionally disturbed little girl's imaginary friend.

Hall is currently starring in his own Showtime television series, Dexter, which revolves around Dexter Morgan, a Miami police forensics expert who moonlights as a vigilante serial killer. The series' first season premiered on October 1, 2006, and its second season began on September 30, 2007. For his work on the series, Hall was nominated for the 2007 Golden Globe Award for Best Actor in a TV Drama and renominated in 2008 for a Golden Globe in the same category. Hall won the 2007 TCA award for Individual Achievement in Drama.