Finneran's biggest film role was as Judy Rose in the remake of George A. Romero's Night of the Living Dead. Her film credits include You've Got Mail, Chicken Little, Liberty Heights, Bewitched, Miss Congeniality 2: Armed and Fabulous, and Death to Smoochy.
She co-starred in television series Wonderfalls. She was also featured as a part of the cast on the Fox show The Inside, in the short-lived CBS sitcom Bram & Alice, and in many guest roles in shows like Frasier, Sex and the City and Oz. In 2007 Finneran was featured in the new series Drive. She played the sister of the main character, Alex Tully (Nathan Fillion).
In an interview for the DVD of the full series of Wonderfalls, Finneran said that when asked if she felt nervous about playing lesbian immigration attorney Sharon Tyler on Wonderfalls she replied, "I'd rather have people think that I'm a lesbian than a lawyer."

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