Sirenia, an iconic marine taxon of cultural and economic importance to tropical coastal communities for millennia, face an uncertain future. All extant species are now designated ‘Vulnerable’ to extinction by the IUCN. Nonetheless, a comprehensive understanding of geographic structuring across the global range of these species is lacking, which impedes our ability to highlight particularly vulnerable populations for conservation priority. In this study, we used ancient DNA to investigate the population structure of the dugong (Dugong dugon), a sirenian with a history of intensive hunting dating back to the Neolithic. We analysed 56 dugong mitogenomes comprising the known historic range in the largest historical whole-genome dataset published to-date for this species. Our results reveal geographically structured and distinct monophyletic clades with contrasting evolutionary histories throughout the range of the dugong. We observed deep-rooted and divergent lineages in the East (Indo-Pacific) and obtain new evidence for the relatively recent dispersal of dugongs into the western Indian Ocean. All populations are significantly differentiated from each other with western Indian populations having at least 10-fold less genetic variation than eastern Indo-Pacific populations. Additionally, we find a significant temporal loss of genetic diversity in western Indian Ocean dugongs since the mid-20th century, as well as a decline in population size beginning ~1,000 years ago. Our results add to the growing body of evidence that dugong populations are becoming ever more susceptible to ongoing human action and global climate change. Thus, we emphasise the urgent need for conservation management of this iconic species.