Since the Reformation in the sixteenth century, Switzerland has been a bi-confessional country. On the base of qualitative empirical data, we explore the evolution of the country’s confessional boundaries from the end of the Ancien Régime to the present. Drawing on the example of the religious education classes in public schools in the French-speaking part of the country, we examine the interplay of geographical and symbolic boundaries, especially regarding the changing role of the State in revealing and shaping confessional boundaries. We identify three major thresholds in the history of religious education. The first is characterized by stabilization of the confessional and political tensions at the end of the nineteenth century. The second is defined by an ecumenical turn in the 1960s. The third occurred at the turn of the twenty-first century when the growing intervention of the State in the field of religious education led to the creation of a compulsory class on religions. By analyzing the social and political processes prompting these reforms we identify three major shifts in the religious and confessional boundaries: First, the symbolic boundary between Catholics and Protestants lost its clarity and is no longer producing social or political divisions. Second, the boundary between the religious and the secular domains is blurred by different conceptions about the public’s role in the public sphere. Third, a new ambivalent boundary between Christianity and the other religions, in particular Islam, can be selectively activated in order to illustrate new symbolic distinctions. Although these changes do not affect the territorial boundaries of the cantons or challenge their autonomy in the regulation between Church and State, the fading of the confessional boundaries, the increasing pluralization of the religious field and the resulting convergence of the cantonal policies point to an increasingly deterritorialized “politics of religions.”