ABSTRACT: The Atlantic herring Clupea harengus has played a pivotal role in the formulation of ideas relating to population structuring in marine fishes, yet considerable uncertainty remains as to the extent to which phenotypic and genetic differentiation coincide in such a highly mobile species. In this study, we examined genetic population structure across the major herring spawning aggregations in the North Sea and adjacent waters over 2 years, 2002 and 2003. We analysed 1660 spawning individuals across 9 microsatellite loci. Data were analysed using several approaches, taking into account the effect of location, year-class and sex, as well as pooling all individuals together, making no assumption as to the number of populations present in the data set. The results suggest the presence of a genetically homogeneous unit off Northern Scotland, and a temporally stable pattern of isolation by distance determined predominantly by the divergence of the English Channel samples and, in 2003, by the Norwegian spring spawners. Our data suggest that the current view of North Sea herring as a unit-stock might be adequate, but confirm the considerable degree of demographic independence of the herring populations in the English Channel. Despite major recent population collapses, genetic data indicated no evidence of bottlenecks affecting the genetic diversity of extant North Sea herring populations. Finally, despite evidence of weak population structuring, we discuss the risks of underestimating population differentiation in marine fish of large population sizes, and with reference to herring population history and dynamics, we attempt to reconcile the existing theories on herring population structure.