Some of his best known roles include Raymond Millbury on Ally McBeal (2001–2002), Grayson Ellis on Cougar Town (2009–2015), and Liam O'Connor on Quantico (2015–2016).

He portrayed Paul Allen in the 1999 film Pirates of Silicon Valley and Raymond Milbury on the television series Ally McBeal from 2001 to 2002.

In 2005, Hopkins guest starred on Fox's show Bones as Temperance Brennan's former professor and lover, Michael Stires, in the episode "The Girl in the Fridge".

In season 1 of the CBS series Cold Case, Hopkins played the role of Assistant District Attorney Jason Kite.

In 2015, Hopkins joined the main cast for Quantico playing the role of Liam O'Connor, a seasoned FBI agent working in the academy.