Global ecological crises threaten human rights, raising questions regarding the legitimacy of international human rights mechanisms. This article addresses this by examining indigenous peoples' ecological claims within the Inter-American human rights system. Endorsing an ecological approach, the article argues that the normative legitimacy of human rights depends on them becoming tools for contesting unjust structures driving socio-ecological destruction. Consequently, the legitimacy of human rights organs will increasingly depend on how well they achieve their normative aims of promoting rights in light of the insights of an ecological approach, particularly as a protection for minority groups, including indigenous peoples. The role of human rights organs, as norm diffusers in supporting actors and movements domestically, highlights the particularized nature of rights struggles, demanding that these organs take into account the contextualized socio-ecological settings in which such struggles arise – which broadly indicates the need for a legal pluralism approach. Such contextualization is particularly relevant for indigenous peoples given their sui generis connection to traditional lands, as well as the increased vulnerability this connection entails. Using three models for approaching indigenous ecological claims – the cultural integrity, self-determination and ecological integrity models – we recognize the pioneering role of both the Inter-American Commission and Court of Human Rights, but suggest that using property rights as the key to all indigenous claims is inadequate. This is because such an approach fails to provide comprehensive protection for indigenous rights – an observation holding true for all three models of indigenous ecological claims, especially in light of the complex geographies of the global ecological crisis.