Domesticated honeybees and wild bees are some of the most important beneficial insects for human and environmental health, but infectious diseases pose a serious risk to these pollinators, particularly following the emergence of the ectoparasitic mite Varroa destructor as a viral vector. The acquisition of this novel viral vector from the Asian honeybee Apis ceranae has fundamentally changed viral epidemiology in its new host, the western honeybee A. mellifera. While the recently discovered Lake Sinai Viruses (LSV) have been associated with weak honeybee colonies, they have not been associated with vector-borne transmission. By combining a large-scale multiyear survey of LSV in Chinese A. mellifera and A. cerana honeybee colonies with globally available LSV-sequence data, we investigate the global epidemiology of this virus.We find that globally distributed LSV is a highly diverse multi-strain virus, which is predominantly associated with the western honeybee A. mellifera. In contrast to the vector-borne deformed wing virus, LSV is not an emerging disease. Instead, demographic reconstruction and strong global and local population structure indicates that it is a highly variable multi-strain virus in a stable association with its main host, the western honeybee. Prevalence patterns in China suggest a potential role for migratory beekeeping in the spread of this pathogen, demonstrating the potential for disease transmission with the man-made transport of beneficial insects.