Abstract Ectoparasites are abundant in natural communities, can have pronounced deleterious fitness consequences to their host and are important vectors of transmissible parasitic disease. Yet very few studies have estimated the magnitude of heritable genetic variation underlying resistance against ectoparasitism, which significantly limits our ability to predict the evolution of this ecologically important character. The present paper reports results of artificial selection for increased resistance in Drosophila nigrospiracula against ectoparasitic, haematophagous mites, Macrocheles subbadius. In this system, which occurs naturally in the Sonoran Desert of North America, ectoparasitism significantly damages the expression of host fitness traits, including longevity, fecundity and male mating success. In the present study, resistance, which was modelled as a threshold trait, responded significantly to selection applied on either sex. Realized heritability, calculated as a mean across four replicates, was estimated to be 0.152 ± 0.014 (SE). The heritability estimate from selection on males did not differ from that on females, but both estimates differed significantly from zero. This documented presence of additive genetic variation for resistance, coupled with knowledge of the fitness consequences of ectoparasitism, indicates that the host population possesses significant evolutionary potential. Selection was applied on the pre-attachment phase, thereby targeting behavioural forms of defence. This study therefore establishes parallels between insects and other animals in their ability to protect themselves and evolve behavioural defences against ectoparasites.