He received his MFA from the Graduate Acting Program at New York University. He has appeared on Broadway in revivals of The Tempest (1995) and The Lion in Winter (1999) and the Tony Award-winning Take Me Out (2003). Off-Broadway he has appeared in The Foreigner (2004) and The Little Dog Laughed (2006).
Huff's screen credits include The Wedding Banquet (1993), Big Daddy (1999), The Good Shepherd (2006), Meek's Cutoff (2010), and Moonrise Kingdom (2012). On television he has been featured in Law & Order, The Wire, Six Degrees, and Fringe. He also stars in the director/writer Kimberly Levin's independent film Runoff.