Cudmore's first major role came in 2003 when he appeared as Piotr Rasputin in the second installment of the X-Men film franchise, X2. He auditioned for the title role in Superman Returns, but lost the role to Brandon Routh. He portrayed the Volturi Felix in The Twilight Saga: New Moon, The Twilight Saga: Eclipse, and The Twilight Saga: Breaking Dawn - Part 1. On July 11, 2012 it was confirmed that Cudmore will portray Master Chief Petty Officer John-117 in the live-action Halo 4: Forward Unto Dawn web series.