Abrahamson was offered a scholarship to study for a PhD in Philosophy in Stanford University. He did not complete this, however, and returned to Ireland to take up filmmaking, initially directing commercials, filming a popular series of adverts for Carlsberg. Abrahamson's first film was Adam & Paul, a black comedy that featured a pair of heroin addicts as they made their way around Dublin in search of a fix. The follow up film to this was 2007's Garage, starring Pat Shortt as a lonely petrol station attendant in rural Ireland. Both films won the IFTA award for best film.

Also in 2007, RTÉ screened Abrahamson's four-part TV miniseries Prosperity, which was written in collaboration with Mark O'Halloran, the co-writer of Adam and Paul and Garage. Like these two films, Prosperity focused on people on the fringes of Irish society, with each one-hour episode focusing on a specific character, including an alcoholic, a single mother, and an asylum seeker. In 2012 Abrahamson won his third IFTA for best film with What Richard Did, which was the most successful Irish film of 2012.

Abrahamson directed the film Frank, which premiered at Sundance Film Festival in January 2014. The film is about an eccentric musician modeled after Frank Sidebottom. It stars Michael Fassbender, Domhnall Gleeson and Maggie Gyllenhall. Abrahamson next directed a film adaptation Emma Donoghue's best-selling novel, Room (2015) for which he received his first Academy Award nomination. The film received very positive reviews.

In 2014, it was announced that Abrahamson would direct an adaptation of Laird Hunt's Civil War novel Neverhome.

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