Crudup attended the University of North Carolina at Chapel Hill, where he received an undergraduate degree, and he continued his passion for acting with the undergraduate acting company, Lab!Theatre. He was a member of the Beta Chapter of Delta Kappa Epsilon. He then studied at the Tisch School of the Arts at New York University, where he earned a Master of Fine Arts in 1994. A year after graduating, he made his debut on Broadway in the Lincoln Center Theater production of Tom Stoppard's Arcadia.
Crudup received a Tony Award nomination for his performance in The Elephant Man on Broadway, as well as for his role as Katurian in the Broadway production of The Pillowman, also starring Jeff Goldblum, which closed on September 18, 2005. From October 2006 through May 2007, he was featured in the first two parts of The Coast of Utopia by Tom Stoppard at Lincoln Center, playing literary critic Vissarion Belinsky, for which he received another Tony Award nomination and subsequent win.
Crudup is currently filming Watchmen with director Zack Snyder in Vancouver, Canada. He is portraying the iconic superhero Doctor Manhattan.
He is on the Board of Directors for The Actors Center in New York City.
| Year | Title | Role | Notes |
|---|---|---|---|
| 1996 | Sleepers | Tommy Marcano | |
| Everyone Says I Love You | Ken | ||
| 1997 | Inventing the Abbotts | John Charles "Jacey" Holt | |
| Grind | Eddie Dolan | ||
| Princess Mononoke | Ashitaka | (voice: English version) | |
| 1998 | Monument Ave. (originally titled Snitch) | Teddy Timmons | |
| Without Limits | Steve Prefontaine | ||
| The Hi-Lo Country | Pete Calder | ||
| 1999 | Jesus' Son | FH | |
| 2000 | Waking the Dead | Fielding Pierce | |
| Almost Famous | Russell Hammond | ||
| 2001 | World Traveler | Cal | |
| Charlotte Gray | Julien Levade | ||
| 2002 | AKA Birdseye | Unknown big role | |
| 2003 | Big Fish | Will Bloom | |
| 2004 | Stage Beauty | Ned Kynaston | |
| 2005 | Trust the Man | Tobey | |
| 2006 | Mission: Impossible III | IMF Operations Director Musgrave | |
| The Good Shepherd | Arch Cummings | ||
| 2007 | Dedication | Henry | |
| 2008 | Pretty Bird | Unknown | |
| 2009 | Watchmen | Doctor Manhattan | post-production |
| Public Enemies | J. Edgar Hoover | post-production |