This study considers what constitutes an appropriate religious education for student teachers of religious education in the second-level sector in the Republic of Ireland. The research adopts an interpretive approach to relevant documentary sources and traces the evolution of how the State and the Catholic Church, given its prominent role in that society, understand the term religious education. This analysis suggests that how the nature and purpose of religious education is understood is a significant context in developing an appropriate religious education for teachers of religious education. It is argued that religious education is best conceived of as a conversational activity that is hermeneutical in nature. How the religious educator is prepared to lead such a conversation is crucial. This concept of religious education is developed by drawing on Thomas Groome’s theological vision of appropriation and Robert Jackson’s educational concept of edification. The argument considers how the study of theology, an essential requirement in the initial teacher education of teachers of religious education according to the Teaching Council of Ireland, can contribute to the religious education of these students. The tradition of theological education, with its focus on how theology is taught, emerges as a significant foundation for a religious education that is appropriate for the students in question. Six principles for such a theological education arise from this research indicating essential elements for an appropriate religious education for future teachers of religious education in the Republic of Ireland and beyond.