Drawing on findings from a study of Indigenous housing in a regional Western Australian city, this paper examines the experiences of Indigenous peoples as a particular set of ‘right bearers’ within the right-to-the-city discourse. In settler-states, colonial discourses of absence, threat, and authenticity have informed policy frameworks that have militated against various Indigenous claims of belonging, rights, and aspiration in relation to urban places. Housing has been a representative domain of struggle in this respect. Consequently, today, Indigenous peoples have disproportionately high rates of dependence on more volatile and discriminatory forms of tenure than their non-Indigenous counterparts. The paper examines the incongruence between State aspirations to move (Indigenous) people along a housing continuum in urban environments, and the actual experiences of Indigenous urban residents, which fix discursively on barriers to such movements. It also traces the deleterious, displacing impacts for urban Indigenous households of the retreat of the State in its role as a landlord for the socio-economically disadvantaged, and in responding to market signals and particular sociological theses regarding poverty, with specific spatial logics. In so doing, we advance two interwoven arguments. First, we assert that Indigenous people face a unique precarity in the Australian urban housing system, which is a result of both colonial and racially discriminatory forces, and economically discriminating processes such as capital concentration and the commodification of land. Second, we contend that this precarity sets many Indigenous people on housing career trajectories that are antithetical to policy intentions.