[9] He often found himself in women's roles, which he says "wasn’t good for my confused adolescent psyche",[10] but also recalls a part in Rosencrantz and Guildenstern Are Dead as being particularly memorable, noting that shouting "Fire!"

[13][15] Dillane is an experienced theatre actor; his notable roles include Archer in The Beaux' Stratagem (Royal National Theatre, 1989), Prior Walter in Angels in America (1993), Hamlet (1994), Clov in Samuel Beckett's Endgame (1996), Uncle Vanya (1998), Henry in Tom Stoppard's The Real Thing (for which he won a Tony Award in 2000), The Coast of Utopia (2002), and a one-man version of Macbeth (2005) directed by Travis Preston.

Dillane is also known for his portrayal of Leonard Woolf in The Hours (2002),[17] English professional golfer Harry Vardon in The Greatest Game Ever Played (2005)[18] and Glen Foy in the Goal!

[24] Dillane, who had not seen the original series, plays Karl Roebuck, the laid-back, experienced British detective to Poésy's humourless French counterpart.

[25] In a second series in 2016, titled The Tunnel: Sabotage, he reprised his role alongside Poésy for a new case involving a deadly airliner crash in the English Channel.

The work, performed live and later adapted for radio broadcast[28] and film,[29] explored the process of filmmaking and the "concept of artifice on the stage" through a single actor, Dillane.

[31] 2015 saw Dillane making other brief returns to stage including a reprise of his reading of Four Quartets in London[32] and a one-off appearance in Tim Crouch's An Oak Tree at the National Theatre.

[27] In October 2023, Dillane signed the Artists4Ceasefire open letter to Joe Biden, President of the United States, calling for a ceasefire of the Israeli bombardment of Gaza.