AimUnderstanding the processes that underlie the distribution of genetic diversity in endangered species is a goal of modern conservation biology. Specifically, how population structure affects genetic diversity and contributes to a species’ adaptive potential remain elusive. The loggerhead sea turtle (Caretta caretta) faces multiple conservation challenges due to its migratory nature and philopatric behaviour.LocationsAtlantic Ocean, Cabo Verde, island of BoavistaMethodsHere, using 4207 mtDNA sequences, we analysed the colonisation patterns and distribution of genetic diversity within a major ocean basin (the Atlantic), a regional rookery (Cabo Verde Archipelago) and a local island (Island of Boavista, Cabo Verde).ResultsHypothesis-driven population genetic models suggest the colonization of the Atlantic has occurred in two distinct waves, each corresponding to major mtDNA lineages. We propose the oldest lineage entered the basin via the isthmus of Panama and sequentially established aggregations in Brazil, Cabo Verde and in the area of USA and Mexico. The second lineage entered the Atlantic via the Cape of Good Hope, establishing colonies in the Mediterranean Sea, and from then on, re-colonized the already existing rookeries of the Atlantic. At the Cabo Verde level, we reveal an asymmetric gene flow maintaining links across nesting groups despite significant genetic structure amongst nesting groups. This structure stems from female philopatric behaviour which could further be detected by weak but significant structure amongst beaches separated by only a few kilometres on the island of Boavista.Main conclusionTo explore demographic processes at diverse geographic scales improves understanding the complex evolutionary history of highly migratory philopatric species. Unveiling the past facilitates the design of conservation programmes targeting the right management scale to maintain a species’ adaptive potential and putative response to human-induced selection.