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He is known for his film and television roles including Stuart Alan Jones in the Channel 4 series Queer as Folk (1999–2000), Tommy Carcetti in the HBO series The Wire (2004–2008), John Boy in the RTÉ series Love/Hate (2010–2011), Petyr "Littlefinger" Baelish in the HBO series Game of Thrones (2011–2017), CIA operative Bill Wilson in The Dark Knight Rises (2012), Janson in Maze Runner: The Scorch Trials (2015) and Maze Runner: The Death Cure (2018), Aberama Gold in the BBC One series Peaky Blinders (2017–2019), Queen's manager John Reid in Bohemian Rhapsody (2018), and Dr. J. Allen Hynek in The History Channel's Project Blue Book (2019–2020). He also provided the voice and motion capture for Paul Serene in the 2016 video game Quantum Break. In 2021, he had a role in the dramatic crime series Mayor of Kingstown.
Gillen has won three Irish Film & Television Awards and has been nominated for a British Academy Television Award, a British Independent Film Award, and a Tony Award.