The question of church-state separation has haunted America since her founding. James Madison and select founding fathers suggest that religions and states are better off when they minimize (or altogether eliminate) their interactions. Many Muslims in Iran, for instance, believe the opposite – aligning state functions with religious motives results in the most effective state. In this paper, I propose a model of thinking about church-state separation in which states and religions must maintain epistemic vulnerability to allow legal, political, and (...) socio-religious change. Simply put, epistemic vulnerability is an attitude of susceptibility to new sources and instances of knowledge. I present institutions as sets of constraints which interact with shared mental models. In this way, I explain how cultural institutions limit and shape individuals’ susceptibility to new knowledge. The more accommodating a religion is to self-assessment when confronted with new knowledge aids in forming institutions that are reliable, efficient, and robust for groups to grow and adopt new ideas. This results in a model of state-religion that highlights the impact on epistemic vulnerability when either religious organizations or state governance expand their responsibilities outside of their proper functions. (shrink)