A Christian imagination of colonial discovery permeated the early modern world, but legal histories developed in very different ways depending on the imperial jurisdictions. This volume explores the contradictions and ironies that emerged in the interactions between biblical warrants and colonial theories of Indigenous “natural” rights. The early debates in the Americas mutated in the British colonies with a range of different outcomes after the American Revolution, and tracking the history of biblical interpretation provides an illuminating pathway through these historical complexities. A ground-breaking legal judgement in the High Court of Australia, Mabo v. Queensland (1992), demonstrates the enduring legacies of debates concerning Indigenous rights over the previous five centuries. Among other peculiarities, the case reveals that the Australian colonies represent the only jurisdiction of the English common law tradition within which no treaties were made with the First Nations. Instead, there is a peculiar development of terra nullius ideology, which can be traced back to the historic influences of the book of Genesis in Puritan thought in the seventeenth century. Bearing in mind the differences between ancient and modern notions of indigeneity, a fresh understanding of this history is timely as settler colonial states reflect on the implications of the United Nations Declaration on the Rights of Indigenous Peoples (2007). The discussion is particularly relevant for the four states who initially voted against the Declaration: the USA, Canada, New Zealand, and Australia.