The Pacific oyster, Crassostrea gigas, was voluntarily introduced from Japan and British Columbia into Europe in the early 1970s, mainly to replace the Portuguese oyster, Crassostrea angulata, in the French shellfish industry, following a severe disease outbreak. Since then, the two species have been in contact in southern Europe and, therefore, have the potential to exchange genes. Recent evolutionary genomic works have provided empirical evidence that C. gigas and C. angulata exhibit partial reproductive isolation. Although hybridization occurs in nature, the rate of interspecific gene flow varies across the genome, resulting in highly heterogeneous genome divergence. Taking this biological property into account is important to characterize genetic ancestry and population structure in oysters. Here, we identified a subset of ancestry-informative makers from the most differentiated regions of the genome using existing genomic resources. We developed two different panels in order to (i) easily differentiate C. gigas and C. angulata, and (ii) describe the genetic diversity and structure of the cupped oyster with a particular focus on French Atlantic populations. Our results confirm high genetic homogeneity among Pacific cupped oyster populations in France and reveal several cases of introgressions between Portuguese and Japanese oysters in France and Portugal.