Australia, Canada and the United States are settler-colonial federations comprising two types of federal units. The first are states/provinces: full, permanent federal partners, securely settler controlled. The second are territories. Historically, territories were “partners in waiting,” slated for federal incorporation once settlers achieved control of the jurisdiction, outnumbering and disempowering Indigenous peoples. The “rights revolution” made achieving control by force less acceptable. Meanwhile, in Australia, Canada and the US, there remain several territories where Indigenous peoples hold significant power. I find today’s remaining territories experience a new way settlers target Indigenous power, not through force but through rights-challenges. Further, I show these rights-challenges provoke “constitutive contests,” the outcome of which are consequential, potentially “re-constituting” territories in a manner fostering settler control. Finally, I explore why territories might be especially vulnerable to re-constitution through settler-rights challenges.