Although North American settler governments face scrutiny over the ecological, social, and ethical shortcomings of environmental policy, many Indigenous Nations are pursuing a resurgence of environmental self-governance according to ancestral principles and practices. On the west coast of Vancouver Island, the reintroduction and prioritized conservation of sea otters by Canada's Department of Fisheries and Oceans (DFO) actively impedes the harvest of culturally and nutritionally significant shellfish species by Nuu-chah-nulth Nations. Integrating a range of qualitative methods, we argue that structural inequities, divergent normative and material priorities, and ontological differences animate a divide between Nuu-chah-nulth and Canadian state governing bodies in sea otter management. The DFO’s unwillingness to accommodate Indigenous knowledge, principles, and priorities in its sea otter management scheme reproduces the unequal power relations of settler colonialism to the detriment of Indigenous food sovereignty and security. We propose to reframe sea otter governance around the Nuu-chah-nulth principles of hišukʔiš c̓awaak (everything is one), ʔiisaak (respect with caring), and ʔuʔaałuk (taking care of). This reorientation is in alignment with the efforts of Indigenous peoples throughout Canada and globally to enact multi-species caretaking through the resurgence of self-governance rooted in ancestral knowledge and wisdom. Ultimately, we argue that a sea otter governance structure centering Nuu-chah-nulth principles, ecological knowledge, and leadership would be well-positioned to lead collaborations and respectful engagement between Indigenous and non-Indigenous Nations.