Thompson received his B from Amherst College in 1983 in Asian Studies and his PhD in Philosophy from the University of Toronto in 1990. He was Professor of Philosophy at the University of Toronto from 2005 to 2013, and held a Canada Research Chair in Cognitive Science and the Embodied Mind at York University from 2002 to 2005. In 2014, he was the Numata Invited Visiting Professor at the Center for Buddhist Studies at the University of California, Berkeley. He has also held invited visiting appointments at the Faculty of Philosophy, Friedrich-Schiller-Universität Jena, the Ecole Polytechnique (Paris), the Center for Subjectivity Research at the University of Copenhagen, and the Department of Philosophy at the University of Colorado, Boulder.
In 2021, Thompson served as the President of the Pacific Division of the American Philosophical Association.
He has co-directed, with Christian Coseru and Jay Garfield, two National Endowment for the Humanities Summer Institutes: Self-Knowledge in Eastern and Western Philosophies (2018) and Investigating Consciousness: Buddhist and Contemporary Philosophical Perspectives (2012).
Thompson also served for many years on planning committees of the Mind and Life Institute.