Aim: Studying clearly delineated populations in marine lakes, islands of sea, we investigated the interplay of habitat size, dispersal potential, and priority effects in shaping marine population genetic structure. Location: Marine lakes and coastal locations in Indonesia, Palau, Papua New Guinea and Australia. Taxon: Mussels (Mytilidae, Brachidontes spp.). Methods: Populations were sampled from four coastal locations and 22 marine lakes of similar age (~8,000 years), yet differing in size (0.04–4.7 km2) and degree of connection to the adjacent sea. While some lakes are highly connected, allowing potential influx of larvae from the sea, others have very limited water exchange. We assessed the phylogeographical structure and demographic history using mitochondrial and nuclear DNA sequence data, and combined this with geometric morphometrics. The effects of lake characteristics on population genetic diversity and structure were tested using linear regression and Mantel tests. Results: Each lake contained one of six distinct genetic lineages, which were characterized by deep phylogenetic splits and significant morphometric differences. These lineages likely represent separate species. The lineages showed similar demographic patterns, with lakes containing founder populations that rapidly expanded and diverged. Genetic diversity within lake populations was significantly correlated with lake area, but not with physical connection to the adjacent sea. Within lineages that occurred in multiple lakes there was strong population structure (average ΦST 0.65), which did not conform to an isolation-by-distance pattern or to the degree of dispersal potential. Main Conclusions: Marine lakes across a gradient of physical isolation show strong population structure and evidence for in situ divergence. We hypothesize that the observed genetic structure is the result of priority effects. In addition, reduction of habitat size appears to reduce genetic diversity, even at very small spatial scales. Our findings are relevant in the context of ongoing alterations to coastal hydrodynamics, which lead to habitat reduction and influence migration among populations at fine spatial scales.