Marine fish species are characterized by a low degree of population differentiation at putatively neutral marker genes. This has been traditionally attributed to ecological homogeneity and a lack of obvious dispersal barriers in marine habitats, as well as to the large (effective) population sizes of most marine fish species. The herring (Clupea harengus) is a case in point – the levels of population differentiation at neutral markers, even across vast geographic areas, are typically very low (FST ≈ 0.005). We used a RAD-sequencing approach to identify 5985 novel single-nucleotide polymorphism markers (SNPs) in herring and estimated genome-wide levels of divergence using pooled DNA samples between two Baltic Sea populations separated by 387 km. We found a total of 4756 divergent SNPs (79% of all SNPs) between the populations, of which 117 showed evidence of substantial divergence, corresponding to FST = 0.128 (0.125, 0.131) after accounting for possible biases due to minor alleles and uneven DNA amplification over the pooled samples. This estimate – based on screening many genomic polymorphisms – suggests the existence of hitherto unrecognized levels of genetic differentiation in this commercially important species, challenging the view of genetic homogeneity in marine fish species, and in that of the Baltic Sea herring in particular.