Acropora is the most diverse and widespread coral genus in the world. Although known for its critical ecological role in shallow-water habitats, its abundance and diversity at upper mesophotic depths have only recently been uncovered. Consequently, little is known about the genetic structuring of mesophotic Acropora populations and their potential ecological and evolutionary relationships with shallow populations. Here, we present the first population genomic evaluation of the depth-generalist coral Acropora aculeus to assess genetic structuring across depths (10 and 40 m) and regions (the Great Barrier Reef (GBR) and the Western Coral Sea (WCS)). We observed strong geographic differentiation between regions, indicating the relative isolation of WCS atolls, with some gene flow occurring from WCS to the GBR, but rarely in the opposite direction. Conversely, we observed no geographic or depth-related genetic structuring within regions, although sample sizes limited the evaluation of local allelic patterns of depth structuring. Our results indicate that widespread connectivity within regions characterizes the broadcast spawning A. aculeus. The lack of depth differentiation should be explored to see whether the wide depth range of some species may be safeguarded against a rapidly changing climate.