[13][14] In 2012 Speleers starred as Jamie in Andy De Emmony's comedy horror film Love Bite, alongside Jessica Szohr and Timothy Spall.

[26][27] On 12 March 2014, it was reported that Speleers was among five actors being considered for a lead role in Star Wars: The Force Awakens, but was cut during the casting process.

[33] That same year, Speleers guest starred in the BBC One miniseries Partners in Crime, an adaptation of two of Agatha Christie's novels, which focused on crime-solving couple Tommy and Tuppence Beresford.

[23][38] The following year he appeared in Andy Serkis' directorial debut, the biopic Breathe, which starred Andrew Garfield and Claire Foy.

[42] In late 2017, Speleers was confirmed to appear in seasons four and five of Starz's time-travel drama series Outlander as Irish smuggler and pirate Stephen Bonnet.

[43][44][45] In 2018 Speleers starred in the dark comedy-horror film Zoo, which centers on a couple in crisis and attempting to reconcile during a zombie pandemic.

[39][46] He went on to feature in Lars von Trier's psychological thriller The House That Jack Built, which premiered at the Cannes Film Festival.

[47] On 20 August 2018, Speleers made his stage premiere in the play Rain Man, portraying the lead role of Charlie Babbitt.

He also appeared as Jack Crusher, a main character and a secret son of the protagonist, in the final season of Star Trek: Picard.

In 2024 Speleers co-starred in the romantic comedy Irish Wish alongside Lindsay Lohan,[60] and was a guest star in an episode of the British television series The Famous Five.