In 1984, Brennan played Collette, one of the main characters in Mike Leigh’s television film, Four Days in July, based on the Troubles in Northern Ireland.

Brennan featured as a guest star in the British television series Cracker in 1995 as a prostitute-hating killer in the episode “Brotherly Love”. Coincidentally, she co-starred in this particular episode with fellow Irish actor Lorcan Cranitch, with whom she would later co-star in Dancing at Lughnasa. Brennan also acted in the much acclaimed Billy trilogy of plays for the BBC Play for Today series with fellow Belfast natives Sir Kenneth Branagh and James Ellis.

In 1999, Brennan played Maisie Madigan in Pearson’s production of Juno and the Paycock at the Gaiety Theatre, Dublin, alongside Michael Gambon whom she had previously appeared with in the 1998 film adaptation of Dancing at Lughnasa. In 2002, Brennan was again nominated for an Olivier award for her performance in the Donmar Warehouse’s 2001 production of The Little Foxes. In 2006, she starred as Sister Aloysius in a production of Doubt at the Abbey Theatre in Dublin.

For RTÉ Radio 1, Brennan played the role of Lucia Joyce in Thomas Kilroy’s In the Garden of the Asylum in 2009.

In 2010, Brennan appeared in the television shows Doctor Who and The Escape Artist, both alongside David Tennant.

In March 2014 it was announced that she had been cast in the role of Kate Keller in Arthur Miller’s All My Sons, playing at the Open Air Theatre, Regent’s Park in May/June 2014, performing alongside Tom Mannion and Charles Aitken, the latter of whom she had previously performed with in The Old Vic’s 2013 production of Sweet Bird of Youth.

In April 2017, she will appear in The Ferryman at the Royal Court Theatre, ahead of a transfer to the Gielgud Theatre in the West End.