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Dennings made her feature film debut in Hilary Duff's Raise Your Voice in 2004 as Sloane, a somber piano student.
Dennings starred in Charlie Bartlett in 2008, the story of a wealthy teenager (Anton Yelchin) who acts as a psychiatrist for his new public high school.
In May 2010, Dennings appeared in a music video for "40 Dogs (Like Romeo and Juliet)", a single by Austin, Texas-based musician Bob Schneider.
Robert Rodriguez directed the video, which was filmed in various locations around Austin.
“I ship it,” Dennings, who previously dated Nick Zano, captioned the image.
She was cast for a five-episode run on The WB's Everwood, but the role was recast with Nora Zehetner.After making her acting debut in an episode of the HBO dramedy series Sex and the City, Dennings has since appeared in films including The 40-Year-Old Virgin (2005), Big Momma's House 2 (2006), Charlie Bartlett (2007), The House Bunny (2008), Nick and Norah's Infinite Playlist (2008), Defendor (2009), Thor (2011) and Thor: The Dark World (2013).From 2011 to 2017, she starred alongside Beth Behrs in the CBS sitcom 2 Broke Girls.The film began production in Orlando, Florida, in February 2011.Dennings stated to The Jewish Journal of Greater Los Angeles that Judaism "is an important part of my history, but, as a whole, religion is not a part of my life." The article went on to say that she considers herself more ethnically and culturally affiliated than religiously so.