Wolfe made her film debut in The Foot Fist Way (2006). She later starred as Nell in Observe and Report (2009). In September 2009, she was cast as Jill in the NBC sitcom 100 Questions, succeeding Joy Suprano, who played the role in the pilot episode. She had a recurring role in the ABC series Cougar Town. In 2011, she signed up for the NBC pilot Lovelives, replacing Amanda Loncar. She co-starred in four never-aired episodes of the cancelled 2012 NBC comedy Next Caller (then titled Next Caller Please). In June 2015, she was cast in the recurring role of improv Teacher Dorothy Durwood in the FXX sitcom You're the Worst. In 2016, Wolfe was cast in a recurring role on TNT's Good Behavior.
