Miller made his feature film debut in Afterschool, playing a teenager who accidentally films the drug-related deaths of two classmates.

Miller starred in We Need to Talk About Kevin and Another Happy Day, earning critical acclaim and nominations at the Gotham Independent Film Awards and the Independent Spirit Awards.

Miller played Patrick in The Perks of Being a Wallflower, winning the Boston Society of Film Critics Award for Best Supporting Actor.

Miller played Barry Allen / The Flash in the DC Extended Universe, appearing in Batman v Superman: Dawn of Justice, Justice League, and The Flash.

Miller played Credence Barebone in the Fantastic Beasts fantasy films, including Fantastic Beasts and Where to Find Them, Fantastic Beasts: The Crimes of Grindelwald, and Fantastic Beasts: The Secrets of Dumbledore.