John Courtney Murray is openly acknowledged as one of the greatest public political thinkers that American Catholicism has produced. His work significantly influenced the Catholic Church's public understanding of the role of religion in a pluralistic society through his contributions to the Declaration on Religious Liberty (Dignitatis Humanae) of the Second Vatican Council. He was even acclaimed in the secular world, appearing on the cover of Time on December 12, 1960. His legacy in the area of church–state relations, however, ran into serious difficulties shortly after his death. Many have alleged that the cause of this nonreception lay in a new religious pluralism in the United States or in a lack of consensus on basic moral or philosophical issues. I will argue, by contrast, that one overlooked, but highly influential, reason for this lack of reception lies in Murray's position on the relationship between nature and grace. The triumph of a competing view in the post-conciliar Catholic Church and wider academy, both in theology and in philosophy, undermined the possibility of Murray's vision finding traction within either realm.