Abstract Marine species often exhibit genetic discontinuities concordant with biogeographic boundaries, frequently occurring due to changes in ocean circulation, bathymetry, coastline topography, and temperature. Here, we used 10 916 single nucleotide polymorphisms (SNPs) to assess the concordance between population genomic differentiation and coastal biogeography in the fishery-important snapper (Chrysophrys auratus) across southeastern Australia. Additionally, we investigated whether spatial scales of assessment and management of snapper align with evidence from population genomics. We detected genomic structure concordant with the region's three biogeographic provinces across snapper from 11 localities (n = 488) between the west coast of South Australia and the south coast of New South Wales. We also detected fine-scale genetic structuring relating to spatial variation in spawning and recruitment dynamics, as well as temporal stability in the genomic signal associated with two important spawning areas. The current management boundaries in the region coincided with either the genetic breaks at bioregional boundaries or with local-scale variation. Our study highlights the value of population genomic surveys in species with high dispersal potential for uncovering stock boundaries and demographic variation related to spawning and recruitment. It also illustrates the importance of marine biogeography in shaping population structure in commercial species with high dispersal potential.