Animal migrations are a fascinating and global phenomenon, yet they are often difficult to study and sometimes poorly understood. Here, we build on classic ecological theory by hypothesizing that some enigmatic spawning migrations across coastal marine habitats can be inferred from the population genetic signature of larval dispersal by ocean currents. We test this assumption by integrating spatially realistic simulations of alternative spawning migration routes, associated patterns of larval dispersal, and associated variation in the population genetic structure of eastern Australian sea mullet (Mugil cephalus). We then use simulation results to assess the implications of alternative spawning destinations for larval replenishment, and we contrast simulated against measured population genetic variation. Both analyses suggest that the spawning migrations of M. cephalus in eastern Australia are likely to be localized (approximately 100 km along the shore), and that spawning is likely to occur in inshore waters. Our conclusions are supported by multiple lines of evidence available through independent studies, but they challenge the more traditional assumption of a single, long‐distance migration event with subsequent offshore spawning in the East Australian Current. More generally, our study operationalizes classic theory on the relationship between fish migrations, ocean currents, and reproductive success. However, rather than confirming the traditionally assumed adaptation of migratory behavior to dominant ocean current flow, our findings support the concept of a genetically measurable link between fish migrations and local oceanographic conditions, specifically water temperature and coastal retention of larvae. We believe that future studies using similar approaches for high resolution and spatially realistic ecological–genetic scenario testing can help rapidly advance our understanding of key ecological processes in many other marine species.