According to the Supreme Court of Canada, Aboriginal title is a property right, albeit of a distinctive kind. Most significantly, the right is subject to an inherent limit: title lands cannot be used in a way that deprives present and future generations of the right to use the land. Aboriginal title is also encumbered by a restraint on alienation, and has its source in Aboriginal legal systems that predate and survive the assertion of Crown sovereignty. In this paper, we argue that these features of Aboriginal title are not burdensome judicial innovations on a property right, but are instead the essential contours of a sovereign right. That is, the Court’s own description of Aboriginal title does not comport with sound theoretical understandings of a property right. Aboriginal title is much more akin to a right of sovereignty—the right to make laws about the use of a territory. Aboriginal title is the right of law-making jurisdiction over the title lands. The existing literature, while edging towards the view that Aboriginal title is a sovereign right, has lacked the unifying theoretical basis needed to decisively dispatch the Court’s property paradigm. In particular, all extant accounts find the inherent limit inexplicable. The account in this article theorizes and explains the inherent limit, as well as all of the sui generis elements of Aboriginal title, and shows their interconnectedness. Our view additionally answers a number of questions that the Court’s property paradigm does not, including: (1) what laws primarily govern title lands; (2) who has standing to question whether any particular use of title land violates the inherent limit; (3) what is the status of private land interests that overlap with Aboriginal title lands; and (4) how should the doctrine of Aboriginal title be updated in light of jurisprudential developments emphasizing that Indigenous peoples never ceded their sovereignty?