In this article, we: (1) advance a theory for how courts should respond to highly political disputes about jurisdictional authority, and (2) assess whether courts can achieve this ideal. Our theory draws from normative realism to argue that courts should push conflict back into the political realm whenever possible—facilitating free and fair dialogue by outlining rules and principles to guide negotiations, while also rejecting zero-sum outcomes when enforcing jurisdictional powers and related rights. We favor this approach because it can generate legitimacy for the legal and political systems by recognizing the judiciary’s limited democratic standing in structural disputes. To ground this argument in actual practice, we assess how the Supreme Court of Canada has managed two streams of highly political jurisprudence related to jurisdictional authority—federalism and Aboriginal rights cases. We show that the Court has increasingly relied on this approach of facilitating dialogue in both areas. While we argue that this approach is particularly well suited to federalism cases, our analysis uncovers negative outcomes in Indigenous case law. The Court’s approach often fails to strongly enforce the constitutional rights of Indigenous peoples, demonstrating that its facilitator role does not adequality account for the power imbalances between the state and Indigenous peoples.