The rise of the city-region concept has focused attention on the nature of territorial politics underpinning city-regionalism. This paper investigates the relationship between territorial politics, city-regionalism and the collective provision of mass transport infrastructure in the USA. It deploys a case study of the Denver region, examining the state and governance structures driving forward FasTracks, a long-term project to expand the Denver Regional Transportation District’s light and commuter rail system. FasTracks represents a programme to retrofit the Denver city-region for integrated mass transit but its funding has fostered tensions around new regionalist governance arrangements. The paper uses the findings of the case study to reflect upon the balance of bottom–up versus top–down geopolitical forces shaping the landscape of city-regionalism in the USA. It emphasises the variety of ways in which struggles around infrastructure provision shape the emergence of new city-regionalist structures inside the competition state.