Cross-species transmission is one of the most significant causes of disease emergence in humans and other species. The Ostreid Herpesvirus type 1 has mostly been detected in the Pacific oyster Magallana gigas in the context of mortality events. However, it has been detected in other mollusc species including the flat oyster Ostrea edulis which raise questions about OsHV-1 host specialization. This study looked at the genetic differentiation of OsHV-1 in Pacific and European flat oysters, and the mechanisms that might underlie this genetic differentiation. To this end, high-throughput deep sequencing was used to analyze forty OsHV-1 genomes to characterize the genetic diversity and the degree of genetic isolation of OsHV-1 viruses from both O. edulis and M. gigas in France as well as to assess the frequency of the virus cross-species transmission. To achieve this, comparative and population genomic, phylogenetic, and phylodynamic approaches were employed. Our findings highlight the significant influence of host species on the genetic diversity and differentiation among OsHV-1. The emergence of OsHV-1 in France seems to be traced back to the introduction of M. gigas, and the virus has since evolved into two distinct lineages following a cross-species event. Moreover, our analysis revealed selection signals in regions responsible for crucial biological functions and domains, indicating the potential for OsHV-1 to adapt and specialize in response to its respective host species. To get further insights into evolutionary processes and host-virus interactions, future research should focus on investigating the coevolution between OsHV-1 and a wider range of host species using phylogenetic approaches.