Hydrothermal vents and hydrocarbon seeps in the deep ocean are rare oases fuelled by chemosynthesis. Biological communities inhabiting these ecosystems are often distributed in widely separated habitats, raising intriguing questions on how these organisms achieve connectivity and whether habitat types facilitate intraspecific divergence. The deep-sea patellogastropod limpet Bathyacmaea nipponica that colonises both vents and seeps across ~2,400 km in the Northwest Pacific is a feasible model to fill such knowledge gaps. In this study, we analysed 123 individuals from four vents and three seeps using a comprehensive method incorporating population genomics and physical ocean modelling. Our results illustrated how the vent and seep populations of B. nipponica have been connected, and how different habitats may have facilitated its population differentiation under the complex influences of seafloor topography and ocean currents. Given that many hydrothermal vents and hydrocarbon seeps are targets of resources extraction (i.e., mining of rare metals and extraction of gas hydrate), our results could also be served as the scientific basis for a better conservation of chemosynthesis-based ecosystems and an effective establishment of marine protected areas.