An understanding of stock recruitment dynamics in fisheries is fundamental to successful management. Pinctada maxima is a bivalve mollusc widely distributed throughout the Indo-Pacific and is the main species targeted for cultured pearl and pearl shell production in Australia. Pearl production in Australia relies heavily on wild-caught individuals, the majority of which come from the Eighty Mile Beach region near Broome in Western Australia. In this study, we used a genotyping by sequencing approach to explore fine-scale patterns of genetic connectivity among inshore shallow and offshore deep populations of P. maxima near Eighty Mile Beach. Our results revealed high-levels of gene flow among inshore and offshore sites and no differences in genetic diversity between depths. Global estimates of genetic differentiation were low (FST = 0.006) but significantly different from zero, and pairwise estimates of genetic differentiation among sites were significant in only 3% of comparisons. Moreover, Bayesian clustering detected no separation of inshore and offshore sample sites, and instead showed all samples to be admixed among sites, locations and depths. Despite an absence of any clear spatial clustering among sites, we identified a significant pattern of isolation by distance. In a dynamic environment like Eighty Mile Beach, genetic structure can change from year-to-year and successive dispersal and recruitment events over generations likely act to homogenize the population. Although we cannot rule out the null hypothesis of panmixia, our data indicate high levels of dispersal and connectivity among inshore and offshore fishing grounds.