The sea cucumber Holothuria (Metriatyla) scabra, known as sandfish, is a high-value tropical echinoderm central to the global bêche-de-mer (BDM) trade. This species has been heavily exploited across its natural range, with overharvesting and ineffective fishery management leaving stocks in the Pacific region heavily depleted. In Fiji, sandfish stocks have not recovered since a 1988 harvest ban, with surveys reporting declining populations and recruitment failure. Therefore, to inform fishery management policy for the wild sandfish resource and to guide hatchery-based restocking efforts, a high-resolution genomic audit of Fijian populations was carried out. A total of 6,896 selectively-neutral and 186 putatively-adaptive genome-wide SNPs (DArTseq) together with an independent oceanographic particle dispersal model were used to investigate genetic structure, diversity, signatures of selection, relatedness and connectivity in six wild populations. Three genetically distinct populations were identified with shallow but significant differentiation (average Fst = 0.034, p≤0.05), comprising (1) Lakeba island (Lau archipelago), (2) Macuata (Vanua Levu), and (3) individuals from Yasawa, Ra, Serua island and Kadavu comprising the final unit. Small reductions in allelic diversity were observed in marginal populations in eastern Fiji (overall mean A = 1.956 vs. Lau, A = 1.912 and Macuata, A = 1.939). Signatures of putative local adaptation were also discovered in individuals from Lakeba island, suggesting that they be managed as a discrete unit. An isolation-by-distance model of genetic structure for Fijian sandfish is apparent, with population fragmentation occurring towards the east. Hatchery-based production of juveniles is promising for stock replenishment, however great care is required during broodstock source population selection and juvenile releases into source areas only. The successful use of genomic data here has the potential to be applied to other sea cucumber species in Fiji, and other regions involved in the global BDM trade. While preliminary insights into the genetic structure and connectivity of sandfish in Fiji have been obtained, further local, regional and distribution-wide investigations are required to better inform conservation efforts, wild stock management and hatchery-based restocking interventions for this valuable invertebrate.