The history of colonialism in Canada has meant both the partition of Indigenous peoples from participating (physically, politically, legally) in the economy and a relentless demand to become assimilated as liberal capitalist citizens. Assimilation and segregation are both tendencies of colonization that protect the interests of white capital. But their respective prevalence seems to depend on the regime of racial capitalism at play. This paper examines the intersection of settler colonization and racial capitalism to shed light on the status of Indigenous economic rights in Canada. I ask, to what extent are Indigenous peoples understood to have economic rights—defined here as the governing authority to manage their lands and resources—and, how we can we analyze these rights to better understand the conjoined meanings of colonialism and capitalism as systems of power today? In this paper, I look at two sites to address this problem: first, I examine how the Supreme Court of Canada has defined the “Aboriginal right” to commercial economies since the patriation of Aboriginal rights into the Constitution in 1982; and, second, I examine how these rights are configured through state resource revenue-sharing schemes with First Nations, in particular from extractive projects, over the past few years. Each case study provides critical material for analyzing the economic opportunities available to First Nations through democratic channels of state “recognition,” as well as when and why tensions between state policies of segregation and assimilation emerge.