Genomic tools are increasingly used to monitor species movement for conservation and management. Understanding Crown-of-Thorns sea star (CoTS) dispersal dynamics is challenging given prolonged planktonic dispersal and cryptic juvenile phases that can sustain large population sizes. Genetic analyses provide tools to understand population relationships, including patterns of connectivity and population spread. However, despite numerous population genetic studies of Indo-Pacific CoTS, the origins of primary outbreaks and population genetic patterns remain unclear, particularly at smaller spatial scales. Here, we used whole-genome sequencing of CoTS populations in the Great Barrier Reef (GBR) to investigate fine-scale population structure across 13 reefs between Cairns and Cooktown, a region known as the initiation box where outbreaks are often first observed. Using over one million loci, we found significant signals for isolation by distance in this region, although there was no discrete population structure as indicated by clustering analyses. However, together with variation in reef-specific diversity indices, these results suggest migration-drift non-equilibrium conditions for these populations. Non-equilibrium genetic signatures may indicate population expansions, bottlenecks and uneven dispersal. Thus, increased sampling across the expanse of the GBR range could enhance understanding of sources of outbreaks, and the connectivity and propagation of outbreaks across the GBR.