Using the language of rights and national self-determination, Aboriginal peoples have mounted a fundamental challenge to Canadian federalism in the past forty years. In order to move beyond the imposed structure of colonial governance, Aboriginal peoples have sought to establish their own form of federal relationship with contemporary Canadian governments and society. While much attention has been devoted to the constitutional and legal dimensions of Aboriginal challenges to state authority, this thesis argues that incremental yet fundamental changes are also taking place in the less visible but nonetheless important arena of policy-making. Aboriginal claims for greater political recognition, combined with the redefinition of the role of the state associated with neoliberal ideas, have led to the emergence of multilevel governance practices between Aboriginal governing authorities and their federal and provincial counterparts. While they do not alter the formal nature of state authority as defined in the constitution, multilevel policy exercises are characterized by growing interdependencies between Aboriginal and non-Aboriginal governing actors, leading to a partial displacement of formal rules of authoritative decision-making in favor of joint decision-making processes and negotiated solutions to policy disputes. Building on comparative analyses of the transformations in the governance regimes of the James Bay Crees and Kahnawa:ke Mohawks, this thesis argues that these multilevel exercises can become transformative spaces for Aboriginal peoples to reshape their relationship with the state and establish themselves as representatives of distinct political communities with their own sources of authority and legitimacy independent of federal and provincial parliaments. As a result, I argue a new form of federalism may well be emerging not through constitutional negotiations or treaty-making exercises, but from below, in everyday practices of governance.