Cunningham began his acting career when he was dared by a friend to audition for a role in a public casting call.

[1][2] Another major role was his portrayal of Brian Curtis, a crooked cop, in the popular, award-winning Canadian series Da Vinci's Inquest.

Other appearances include the Canadian series Flashpoint[1] and in Sanctuary,[3] where he plays the husband of a biologist friend of Henry Foss.

His most notable role is as John Pope on Falling Skies[1][4][2] He also gained critical acclaim[citation needed] as Master of Ceremonies, Julian Slink in the Syfy series Blood Drive.

He starred as an anti-clone activist named Tripp in the 2000 thriller The 6th Day,[3] and as the character McCabe in the 2005 film Elektra.