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It has been uncontroversial in Canada since the Supreme Court of Canada’s decision in Haida Nation v British Columbia (Minister of Forests) that the Crown bears a constitutional duty to consult Indigenous peoples before proceeding with any conduct that threatens potential or unproven Indigenous rights or title. This duty is rooted in the honour of the Crown and is important to the broader goal of reconciliation between Indigenous and non-Indigenous Canadians. But section 35 of the Constitution Act, 1982 mentions neither the honour of the Crown nor the duty to consult. The conceptual foundations of the duty are unclear and remain undertheorized, leaving courts, Indigenous peoples, the Crown, and private industry to wonder precisely what consultation should involve. This article attempts to fill this theoretical gap. First, it argues, as an analytical matter, that the duty to consult is most coherently understood to flow from a commitment to creating space within the existing structures of Canadian democracy for the exercise of political sovereignty by Indigenous peoples. Second, the article makes the normative argument that this is the correct way to understand the duty. Canada’s historical failure since contact to recognize Indigenous sovereignty in any politically meaningful way has perpetuated a sovereignty deficit in Canada. Reconciliation, in turn, requires erasing this sovereignty deficit. Crown consultation with Indigenous peoples is one way to restore some degree of political sovereignty to Indigenous peoples, by holding the Crown more directly accountable to Indigenous communities. If these procedural protections for unproven Indigenous rights and title are to promote reconciliation, it must be shaped and informed by the extent to which consultation increases Crown accountability to Indigenous peoples and allows Indigenous peoples to act as sovereign, politically autonomous nations. This proceduralized understanding of section 35, however, should not be allowed to undermine the substantive protections that section 35 entrenches for existing Indigenous rights and title.