AbstractSea lampreyPetromyzon marinusis an anadromous and semelparous fish without homing behaviors. Despite being a freshwater, free‐living organism for a large part of their life cycle, its adulthood is spent as a parasite of marine vertebrates. In their native European range, while it is well‐established that sea lampreys comprise a single nearly‐panmictic population, few studies have further explored the evolutionary history of natural populations. Here, we performed the first genome‐wide characterization of sea lamprey's genetic diversity in their European natural range. The objectives were to investigate the connectivity among river basins and explore evolutionary processes mediating dispersal during the marine phase, with the sequencing of 186 individuals from 8 locations spanning the North Eastern Atlantic coast and the North Sea with double‐digest RAD‐sequencing, obtaining a total of 30,910 bi‐allelic SNPs. Population genetic analyses reinforced the existence of a single metapopulation encompassing freshwater spawning sites within the North Eastern Atlantic and the North Sea, though the prevalence of private alleles at northern latitudes suggested some limits to the species' dispersal. Seascape genomics suggested a scenario where oxygen concentration and river runoffs impose spatially varying selection across their distribution range. Exploring associations with the abundance of potential hosts further suggested that hake and cod could also impose selective pressures, although the nature of such putative biotic interactions was unresolved. Overall, the identification of adaptive seascapes in a panmictic anadromous species could contribute to conservation practices by providing information for restoration activities to mitigate local extinctions on freshwater sites.