Over the past two decades, the organisation of religious education classes in Switzerland has undergone profound reforms. Amid the increasing secularisation and pluralisation of the religious landscape, many cantons have introduced a compulsory course that falls under the responsibility of the state and is aimed at teaching basic knowledge about a variety of religions. These reforms have enabled a harmonisation of the syllabi for religious education across the country and have prompted the adaptation of teacher training programmes. Because of the many diverse social expectations surrounding these new courses and the diverse academic traditions in the field of religious education, however, a unified conception of these courses is still absent. In this article, we discuss the ongoing construction of religious education teachers' professional ethos within this fluid context. In particular, we discuss the perspective of teacher trainers on pragmatic questions concerning religious plurality and the place of teachers' and pupils' personal (religious) experiences in the classroom, and pay attention to different representations of 'religion' and distinct ideas regarding the purpose of these courses as they have a major impact on the professional attitudes expected from teachers.