Clerkin has appeared in various TV shows including Smack the Pony, The Inbetweeners and The IT Crowd, and feature films Gangster No.
He played alongside Sharon Horgan in BAFTA nominated sitcom Pulling (2006–2009), and appeared in the soap opera EastEnders (2009) as Joel Reynolds.
He played Clarkey in the police satire Babylon (2014), directed by Danny Boyle, and appeared in the BBC sitcom Count Arthur Strong (2014).
He plays Father Pyrlig in the Netflix drama The Last Kingdom (2017-2022) and Seven Kings Must Die (2023), and Detective Sergeant Flynn in the BBC surveillance thriller The Capture (2019–).
In 2019 he won Best Actor award at the Tallinn Black Nights Film Festival for his performance in Gerard Johnson's psychological thriller Muscle (2019).