Despite being critically endangered, the at-sea behaviour of hawksbill turtles (Eretmochelys imbricata) remains insufficiently understood to support a global conservation strategy. Habitat location and spatial use are poorly documented, which is particularly true for the globally important Australian hawksbill population. We equipped 10 adult female hawksbill turtles nesting on Groote Eylandt, northern Australia, with Fastloc GPS and Argos satellite transmitters. We quantified fine-scale habitat use and area-restricted search behaviour, and located potential feeding and developmental habitats by simulating hatchling turtle dispersal patterns by using a particle-tracking hydrological model. During the breeding season, females mostly remained near their nesting site. Post-breeding, all turtles migrated to foraging sites on the Australian continental shelf, primarily in the Gulf of Carpentaria in coastal seagrass pastures, but also offshore near coral-reef platforms. The distribution of adult foraging grounds was similar to simulated dispersal patterns of hatchling turtles from distant rookeries, thus highlighting the ecological significance of the Gulf of Carpentaria for hawksbill turtles. Although this hawksbill turtle population is likely to be endemic to Australian waters, national and international conservation initiatives are required to mitigate sources of anthropogenic mortality (e.g. illegal tortoise-shell trade, incidental captures in fishing gear, marine debris, seabed mining exploitation).