Little is known about the genetic basis differentiating resident and anadromous forms found in many salmonid species. Using a medium-density SNP array, we documented genomic diversity and divergence at 2336 genetically mapped loci among three pairs of North American anadromous and freshwater Atlantic salmon populations. Our results show that across the genome, freshwater populations have lower diversity and a smaller proportion of private polymorphism relative to anadromous populations. Moreover, differentiation was more pronounced among freshwater than among anadromous populations at multiple spatial scales, suggesting a large effect of genetic drift in these isolated freshwater populations. Using nonhierarchical and hierarchical genome scans, we identified hundreds of markers spread across the genome that are potentially under divergent selection between anadromous and freshwater populations, but few outlier loci were repeatedly found in all three freshwater-anadromous comparisons. Similarly, a sliding window analysis revealed numerous regions of high divergence that were nonparallel among the three comparisons. These last results show little evidence for the parallel evolution of alleles selected for in freshwater populations, but suggest nonparallel adaptive divergence at many loci of small effects distributed through the genome. Overall, this study emphasizes the important role of genetic drift in driving genome-wide reduction in diversity and divergence in freshwater Atlantic salmon populations and suggests a complex multigenic basis of adaptation to resident and anadromous strategies with little parallelism.