Adiaphora (‘indifferent matters’) and permissive natural law both conceptually pointed towards an arena of liberty in which the individual remained free to take up (or not) particular courses of action. In the Reformation debates over the external regulation of Christian freedom for the maintenance of peace and order, these two concepts became freighted with political significance; but they also in turn shaped attitudes over when and where obedience was due in relation to the civic regulation of liberty. Tudor apologetics deployed both ideas in order to defend the English Reformation, especially the claim of the royal supremacy to have due authority to regulate ecclesiastical affairs in indifferent matters, limiting Christian freedom and requiring obedience. By situating these debates within the context of the conceptual development of adiaphora and permissive natural law from their original philosophical roots through to the Reformation, this article establishes the genealogy of claims that defined such apologetics. After surveying the seemingly intractable dilemmas in the thought of Thomas Starkey and John Whitgift over why obedience to lay ecclesiastical supremacy was due, this article considers the radical return to the permissive natural law traditions of the medieval period in the Elizabethan conformist thought of Richard Hooker. In this return, Hooker supplanted divine permissions and scriptural principles as the guide for the proper regulation of indifferent matters with an appeal to the light of reason as the divine instrument through which binding human laws are made to govern society and limit freedom for the public good, even in the life of the national church.