He has also had an extensive stage acting career, appearing mostly on Broadway. He has been nominated four times for a Tony Award for his acting, and won once, for his role in Tom Stoppard's The Coast of Utopia in 2007.
From 1998 to 2005, Crudup was the narrator for "Priceless", a popular U.S. television ad campaign for MasterCard.
Crudup was born in Manhasset, New York. His parents, Georgann (née Gaither) and Thomas Henry Crudup III, divorced during his childhood, and later remarried, before divorcing a second time. On his father's side, he is a descendant of Congressman Josiah Crudup of North Carolina. His maternal grandfather was William Cotter "Billy" Gaither, Jr., a well-known Florida trial lawyer, and his maternal grandmother later remarried to Episcopal bishop James Duncan. Crudup has two brothers: Tommy, an executive producer, and Brooks, also a producer. He left New York with his family when he was about eight years old, first living in Texas, then in Florida. He graduated from Saint Thomas Aquinas High School in Fort Lauderdale, Florida in 1986.
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 also acted for UNC-STV's most popular show, General College. He was a member of the Beta Chapter of Delta Kappa Epsilon. He then studied at the Graduate Acting Program at New York University's Tisch School of the Arts, where he earned a Master of Fine Arts degree in 1994.
Crudup began acting in films such as 1996's Sleepers, 1997's Inventing the Abbotts and 1998's Without Limits, where he played the role of running legend and Olympian Steve Prefontaine. His first role in an animated feature was in 1999's English release of Princess Mononoke, in which he starred as Ashitaka. He then played Russell Hammond, the lead guitar player of the fictional band Stillwater in Cameron Crowe's Almost Famous (2000). In 2006's The Good Shepherd, he played British spy Arch Cummings, a stand-in for Kim Philby. The same year, he played a supporting role in Mission: Impossible III.
Crudup completed Watchmen with director Zack Snyder in Vancouver, British Columbia. He portrayed the superhero Doctor Manhattan. He portrayed former U.S. Secretary of the Treasury Timothy Geithner in a TV film about 2008's financial crisis, Too Big to Fail (2011).
A year after graduating, he made his debut on Broadway in the Lincoln Center Theater production of Tom Stoppard's Arcadia.
Crudup received a 2002 Tony Award nomination for Best Actor in a Play for his performance as the title character in The Elephant Man on Broadway, as well as a 2005 nomination 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 a 2007 Tony Award for Best Featured Actor in a Play.
He starred in The Metal Children, an off-Broadway play written and directed by Adam Rapp in 2010.
In 2011, Crudup received a Tony Award nomination for Featured Actor in a Play for his role in the Broadway revival of Arcadia.
In August 2013, he co-starred with Ian McKellen and Patrick Stewart in the Harold Pinter play No Man's Land as well as in Waiting for Godot at the Berkeley Repertory Theatre. The shows transferred to The Cort Theatre in New York City, where they ran in repertory until March 2014.
From 1998 to 2005, Crudup was the narrator for the "Priceless" television ads for MasterCard. He said in 2005 that appearing in the ads "changed my life", in that they gave him the financial freedom to pursue the acting work that he wanted to do.
He appeared as Zartan in the 2009 parody video The Ballad of G.I. Joe on the website Funny or Die.
In February 2012, Crudup narrated a five-part television series on the first (of three) stages of the renovation of Madison Square Garden, which was televised on the Madison Square Garden Network.
He is on the Board of Directors for The Actors Center in New York City.
From 1996 to 2003, Crudup dated actress Mary-Louise Parker, with whom he has a son, William Atticus Parker (born January 7, 2004). He left Parker while she was 7 months pregnant and started a relationship with his Princess Mononoke and Stage Beauty co-star Claire Danes. They broke up four years later.2007: Tony Award, for The Coast of Utopia: Part 1 – Voyage
2001: OFCS Award, for Almost Famous
2000: Paris Film Festival, for Jesus' Son
1999: Western Heritage Award, for The Hi-Lo Country
1998: NBR Award, for The Hi-Lo Country
2011: Tony Award, for Arcadia
2005: Tony Award, for The Pillowman
2002: Tony Award, for The Elephant Man
2002: Satellite Award, for Charlotte Gray
2001: Screen Actors Guild Award, for Almost Famous
2000: Blockbuster Entertainment Award, for Almost Famous
2000: MTV Movie Award, for Almost Famous
1999: Independent Spirit Award, for Jesus' Son