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Stephen Dillane trained at the Bristol Old Vic Theatre and worked in Coventry, Manchester and Chester, and then at the National Theatre, where he appeared in The Beaux Stratagem, Dancing at Lughnasa, Long Day's Journey Into Night and Angels in America. At the Royal Court, Dillane appeared in Hush and at the Gielgud Theatre in the title role of Hamlet. In addition, he appeared in Endgame at the Donmar Warehouse, in Hurlyburly at the Old Vic, in the title role of Uncle Vanya for the Royal Shakespeare Company at the Young Vic and in Tom Stoppard's The Real Thing at the Donmar Warehouse in the West End and on Broadway, where he won the Tony Award as Best Actor. Most recently, he earned great acclaim for his performance in the new Tom Stoppard trilogy Coasts of Utopia at the Royal National Theatre.

On British television he has been seen in numerous productions, including Dennis Potter's Christabel, the series The Rector's Wife, David Hare's production Heading Home, D.H. Lawrence's The Widowing of Mrs. Holroyd and Kings in Grass Castles, for which he was awarded Best Actor in a Leading Role by the Australian Film Institute. Most recently, he appeared in the miniseries, The Cazalets.

Dillane's film credits include Welcome to Sarajevo, Firelight, Spy Game, The Darkest Light, Franco Zeffirelli's Hamlet and the title role in Jonathan Demme's The Truth About Charlie.