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We explore two special challenges indigenous peoples pose to the idea of sovereigns as trustees for humanity. The first challenge is rooted in a colonial history during which a trusteeship model of sovereignty served as an enabler of paternalistic colonial policies. The challenge is to show that the trusteeship model is not irreparably colonial in nature. The second challenge, which emerges from the first, is to specify the scope and nature of indigenous peoples’ sovereignty within the trusteeship model. Whereas the interaction between states and foreign nationals is the locus of cosmopolitan law, the relationship between states and indigenous peoples is distinctive. In the ordinary cosmopolitan case, foreign nationals do not purport to possess legal authority. Indigenous peoples often do make such a claim, pitting their claim to authority against the state’s. We discuss how international law has attempted to come to grips with indigenous sovereignty by requiring states to include indigenous peoples in decision-making processes that affect their historical lands and rights. A crucial fault line in the jurisprudence, however, separates a duty to consult indigenous peoples from a duty to acquire their free, prior and informed consent (FPIC). The latter but not the former recognizes that indigenous peoples possess a veto over state projects on their lands, in effect recognizing in them a limited co-legislative power. We focus on recent jurisprudence from the Inter-American Court of Human Rights, and consider whether either the duty to consult or FPIC are enough to dispel the shadow of the trusteeship model’s colonial past. We suggest that they are a move in the right direction, and that implicitly they represent international law’s recognition that states are no longer the sole bearers of sovereignty at international law. In limited circumstances, international law recognizes indigenous peoples as sovereign actors.