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The ectoparasite <i>Varroa destructor</i> is the greatest biotic threat of honey bees <i>Apis mellifera</i> in vast regions of the world. Recently, the study of natural mite-resistant populations has gained much interest to understand the action of natural selection on the mechanisms that limit the mite population. In this study, the components of the <i>A. mellifera</i>–<i>V. destructor</i> relationship were thoroughly examined and compared in resistant and susceptible honey bee populations from two regions of Uruguay. Mite-resistant honey bees have greater behavioral resistance (hygienic and grooming behaviors) than susceptible honey bees. At the end of the summer, resistant honey bees had fewer mites and a lower deformed wing virus (DWV) viral load than susceptible honey bees. DWV variant A was the only detected variant in honey bees and mites. Molecular analysis by Short Tandem Repeat showed that resistant honey bees were Africanized (<i>A. m. scutellata</i> hybrids), whereas susceptible honey bees were closer to European subspecies. Furthermore, significant genetic differentiation was also found between the mite populations. The obtained results show that the natural resistance of honey bees to <i>V. destructor</i> in Uruguay depends on several factors and that the genetic variants of both organisms can play a relevant role.