The Pacific cupped oyster is genetically subdivided into two sister taxa, Crassostrea gigas and Crassostrea angulata, which are in contact in the north-western Pacific. The nature and origin of their genetic and taxonomic differentiation remains controversial due the lack of known reproductive barriers and the high degree of morphologic similarity. In particular, whether the presence of ecological and/or intrinsic isolating mechanisms contributes to species divergence is unknown. The recent co-introduction of both taxa into Europe offers a unique opportunity to test how genetic differentiation is maintained under new environmental and demographic conditions. We generated a pseudochromosome assembly of the Pacific oyster genome using a combination of BAC-end sequencing and scaffold anchoring to a new high-density linkage map. We characterized genome-wide differentiation between C. angulata and C. gigas in both their native and introduced ranges, and showed that gene flow between species has been facilitated by their recent co-introductions in Europe. Nevertheless, patterns of genomic divergence between species remain highly similar in Asia and Europe, suggesting that the environmental transition caused by the co-introduction of the two species did not affect the genomic architecture of their partial reproductive isolation. Increased genetic differentiation was preferentially found in regions of low recombination. Using historical demographic inference, we show that the heterogeneity of differentiation across the genome is well explained by a scenario whereby recent gene flow has eroded past differentiation at different rates across the genome after a period of geographical isolation. Our results thus support the view that low-recombining regions help in maintaining intrinsic genetic differences between the two species.