His film roles include CIA operative Bill Wilson in The Dark Knight Rises (2012), Dr. Frank Harte in Calvary (2014), Janson in Maze Runner: The Scorch Trials (2015) and Maze Runner: The Death Cure (2018), Robert in Sing Street (2016), and John Reid in Bohemian Rhapsody (2018).

[4] Gillen began his acting career as a teenager, joining the National Youth Theatre at the age of fourteen[3] and playing Nick Bottom in a production of A Midsummer Night's Dream at the Project Arts Centre when he was sixteen.

In 2011, Gillen began playing Petyr "Littlefinger" Baelish on the HBO series Game of Thrones, for which he received his second Irish Film & Television Award nomination.

[15] Gillen's character was particularly noted by some Internet circles for his delivery of supposedly awkward dialogue in the film's opening plane scene, especially by users of 4chan's /tv/ board.

Thus, he subsequently became the subject of an Internet meme popular among /tv/ users known as "Baneposting",[16] which references the dialogue between Wilson and Tom Hardy's character Bane in said scene.

[17][18] The same year, Gillen also starred in the British spy-drama Shadow Dancer, and was announced as the new host of the music show Other Voices.

[21] He shared a Screen Actors Guild Award nomination with the cast of Game of Thrones for Outstanding Performance by an Ensemble in a Drama Series.

[23] Gillen played Queen's manager John Reid in the biopic Bohemian Rhapsody, which was released on 2 November 2018.

Gillen played Dr. J. Allen Hynek, a brilliant and underappreciated college professor who is recruited by the U.S. Air Force to spearhead an operation named Project Blue Book.