He began directing plays in Dublin in the early 1990s, reached London's West End by 1996 and eventually become an associate director at the Donmar Warehouse.

In 2000, he directed Come and Go as part of the Beckett on Film series and made his feature debut Intermission (2003), a comedy drama set in Dublin, starring Colin Farrell, Cillian Murphy and Kelly Macdonald, based on a screenplay by playwright Mark O'Rowe.

"[4] In 2007, Crowley reteamed with O'Rowe for the thought-provoking BAFTA-winning drama Boy A, about a young man's return to civilian life after imprisonment for a brutal childhood killing, which was made for British television but was released theatrically in the US the following year.

He directed Neve Campbell and Cillian Murphy in the West End production of Love Song in 2006-7, and in 2007 filmed a television version of Harold Pinter's Celebration starring Michael Gambon, Stephen Rea and Colin Firth.

In July 2016, it was announced that Crowley will direct the screen adaptation of Donna Tartt's Pulitzer Prize-winning novel The Goldfinch for Warner Bros. and RatPac Entertainment, starring Ansel Elgort, Oakes Fegley, Aneurin Barnard and Finn Wolfhard.