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At the urging of the late Frederick Crosson, the Center for Philosophy of Religion was established in the fall of 1976 in order to promote, support and disseminate scholarly work in philosophy of religion and Christian philosophy. A few years later, Crosson resigned as director and Alvin Plantinga, then-John A O'Brien Professor of Philosophy, took over the directorship of the Center. In 2002, Plantinga retired as director, handing the reigns to Thomas P. Flint. Flint was director of the Center from 2002 until 2008, when he became editor of Faith and Philosophy. Michael C. Rea and Samuel Newlands currently co-direct the Center.

In its early years, the Center pursued two kinds of projects. It held biannual conferences on topics in philosophy and theology, religion and science, and the nature of Christian scholarship. The Center also awarded fellowships to junior and senior faculty working in theology and philosophy of religion. Recently, the Center has become more prominent in promoting research initiatives in philosophy of religion, philosophical theology, and interdisciplinary topics in collaboration with the social sciences. Over roughly the last decade, the Center has received several multi-million dollar grants from the John Templeton Foundation to investigate and further human understanding of the problem of evil, analytic theology, religious experience, and hope and optimism. Funding from these grants supports interdisciplinary research in social science, philosophy, and theology, residential fellowships at Notre Dame, conferences, high quality media, and strategic public engagement initiatives.