As general editor of The New Polis from the beginning of 2018 to the spring of 2021, I initiated a broad call for work related to the Doctrine of Discovery. At our conference, “Decoloniality and Disintegration of Western Cognitive Empire – Rethinking Sovereignty and Territoriality in the 21st Century,” I gave a brief introduction to the history of the Doctrine of Discovery. The aim of this paper is to outline the history and persistent influence of the Doctrine today, as well as to suggest its undoing. In the end, I argue that the overturning of the 1823 Johnson v. M’Intosh decision, along with a more definitive end to its international counterpart, the Monroe Doctrine, provides achievable groundwork for decolonizing while simultaneously opening ways to return land to Indigenous peoples. Although it may seem an impossible task to some, the precedent of effectively overruling Plessy v. Ferguson (1896) with Brown v. Board of Education (1954) was brought about by decades of work and research. The critical conversation around the Doctrine of Christian Discovery is still in its early stages, obscured by outdated secularization narratives and rhetorical erasure of American Indians. This work is also especially timely with the recent ratification of the 2007 Declaration on the Rights of Indigenous Peoples by the United States because deciding how these recent international commitments will be made demands a thorough assessment of the past.