The cupped oysters Crassostrea angulata and Crassostrea gigas have been sequentially introduced in Europe from their native Pacific area for aquaculture purposes. Ongoing viral epidemic disease is responsible for large losses in oyster aquaculture production throughout Europe. In parallel with current efforts in developing selection programs for disease resistance, it becomes critically important to characterize genetic diversity patterns in both native and introduced areas. With the advent of next generation sequencing techniques, the power to resolve the fine-scale genetic structure at a genome-wide scale opens to new perspectives towards genetic resource management. Here, we present a genome-wide screen of genetic variation that combines SNP genotyping and RADsequencing approaches. Our results, based on more than 18,000 SNP markers, improve our comprehension of the population structure and provide a powerful subset of highly informative markers for stock assignment. As these markers were also used in QTL mapping approaches, these new genomic resources will orientate the choice of breeders in selection programs in order to maximize the natural genetic variance involved in pathogen resistance.