Varroa destructoris an ectoparasitic mite of honeybees which vectors a range of pathogenic viruses, the most notable being Deformed wing virus (DWV). Mites parasitise bees during pupal development and male honeybees, drones, have a longer development cycle than female workers (24 versus 21 days), allow for more progeny mites to develop per foundress (1.6–2.5 compared to 0.7–1.45). How this longer exposure time influences evolution of the transmitted virus population is unknown. Using uniquely tagged viruses recovered from cDNA we investigated the replication, competition and morbidity of DWV genotypes in drones. Assays examining virus replication and morbidity revealed drones are highly susceptible to both predominant genotypes of DWV. In virus passage studies using an equimolar inocula of major DNA genotypes and their recombinants, the recombinant form dominated but did not reach 100% of the virus population within 10 passages. Using anin-silicomodel of the virus–mite–bee system we examined bottlenecks during virus acquisition by the mite and subsequent injection of viruses into the host, which may play a significant role in shaping virus diversity. This study furthers our understanding of the variables influencing DWV diversity changes and provides insight into areas of future research in the mite–virus–bee system.