Abstract: The principle of Indigenous sovereignty acknowledges the liberal imperative of state authority, and yet simultaneously transforms it. Fundamental principles of sovereignty embedded in Westphalian ideas of state and nation-state are counterpoised against in other rationalities—including concepts of cultural rights, human security and more localized sovereignties. Canada’s experience in laying claim to both the internal waters of the Canadian Northwest Passage, and its more recent claim to the extended continental shelf in the Arctic Ocean, are a case in point. In both of these cases Indigenous sovereignty challenges the right of the Canadian state to make such claims without the explicit permission of Inuit peoples. Yet, gaining such permission supports conventional sovereign claims much the way is conventionally associated with the Peace of Westphalia, even if history was more complicated and less immediate in its compliance with what became conflated over time with Westphalian ideals. Meanwhile, land claims treaties in Canada’s Arctic along with new understandings of climate change and human security support a reassessment of sovereignty in practice, and an expansion from the Westphalian ideal to a post-Westphalian synthesis of Indigenous and state sovereignties. Can we still call such arrangements “liberal”, and is decolonization consistent within a framework of liberal views of state sovereignty? The Inuit experience at the nexus of Indigenous and state sovereignty suggests we can indeed, and that Canada’s evolving conception of sovereignty re-introduces tribal sovereignty as a pillar of the new, post-Westphalian order. While similar processes are under way across the Indigenous world, whether in the Far North or Global South, the experience in Arctic North America sheds important light on the evolution of sovereignty in both theory and practice as Indigenous values and conceptions are increasingly recognized and embraced by the sovereign states that emerged in their homelands through colonial state expansion.