The Canadian constitutional text speaks to Canada’s Indigenous populations in different places including in the federal power provisions of the Constitution Act, 1867, in the Canadian Charter of Rights and Freedoms and the Aboriginal Rights section of the Constitution Act, 1982. Each of these is under-inclusive. This paper draws on collaborative research and policy development work with Indigenous political organizations representing off-reserve and non-status Indigenous populations. The paper reports that since the 1970s, Indigenous self-governance organizations outside of the scope of the Indian Act have participated in settler constitutional law-making as well as Indigenous law-making addressing identity and recognition. In doing so, these organizations are constantly navigating the interface between settler law and Indigenous self-governance and have developed sophisticated and hyper-vigilant approaches to this ongoing challenge.