In the present study, we used high-throughput deep sequencing to characterize the genetic diversity of OsHV-1 found in both O. edulis and M. gigas in France and Sweden. To this end, we sequenced and assembled 40 new OsHV-1 genomes. Using these data and previously gathered information about genotypes circulating in different host species, our aims were to (i) describe OsHV-1 genomic diversity patterns in both species, (ii) estimate the genetic isolation between viruses infecting both species and (iii) determine if OsHV-1 cross-species transmission occur and at which frequency. To do so, we applied a combination of comparative and population genomic, phylogenetic and phylodynamic approaches and discussed results in the context of current knowledge of OsHV-1 molecular epidemiology.