Talley was born in Chicago, Illinois. She graduated from Kennedy High School in 1981.
In her twenties, Talley performed improv comedy in Chicago at the Improv Institute and The Second City. Talley and her husband, Tom Kenny, were both cast members of the cult short-lived FOX Network sketch comedy show The Edge from 1992 to 1993 and sketch comedy show Mr. Show from 1995 to 1998. They also appeared together in the May 1996 video for "Tonight, Tonight" by The Smashing Pumpkins as a married couple who take a honeymoon on the moon.
Since 1999, Jill Talley has played Karen Plankton on SpongeBob SquarePants. She was promoted to a main cast member in the credits of its 2004 film adaptation. Talley's other vocal work includes playing several characters on Camp Lazlo (Gretchen, Nina, and Ms. Mucus) and playing Sarah Dubois on the Adult Swim show The Boondocks. She also voiced Lady Granite in the Plastic Man DC Nation Shorts and Maja the Sky Witch in the Adventure Time episode "Sky Witch”.

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