Butler attended Bennington College before transferring to Yale University, where they studied philosophy and received a Bachelor of Arts in 1978 and a Doctor of Philosophy in 1984. They spent one academic year at Heidelberg University as a Fulbright Scholar. Butler taught at Wesleyan University, George Washington University, and Johns Hopkins University before joining University of California, Berkeley, in 1993. In 2002 they held the Spinoza Chair of Philosophy at the University of Amsterdam. In addition, they joined the department of English and Comparative Literature at Columbia University as Wun Tsun Tam Mellon Visiting Professor of the Humanities in the spring semesters of 2012, 2013 and 2014 with the option of remaining as full-time faculty.