Intraspecific specialization by insect herbivores on different host plant species contributes to the formation of genetically distinct “host races,” but the effects of plant virus infection on interactions between specialized herbivores and their host plants have barely been investigated. Using three genetically and phenotypically divergent pea aphid clones (Acyrthosiphon pisum L.) adapted to either pea (Pisum sativum L.) or alfalfa (Medicago sativa L.), we tested how infection of these hosts by an insect-borne phytovirus (Bean leafroll virus; BLRV) affects aphid performance and preference. Four important findings emerged: 1) mean aphid survival rate and intrinsic rate of population growth (R_m) were increased by 15% and 14%, respectively, for aphids feeding on plants infected with BLRV; 2) 34% of variance in survival rate was attributable to clone × host plant interactions; 3) a three-way aphid clone × host plant species × virus treatment significantly affected intrinsic rates of population growth; and 4) each clone exhibited a preference for either pea or alfalfa when choosing between noninfected host plants, but for two of the three clones tested these preferences were modestly reduced when selecting among virus-infected host plants. Our studies show that colonizing BLRV-infected hosts increased A. pisum survival and rates of population growth, confirming that the virus benefits A. pisum. BLRV transmission affected aphid discrimination of host plant species in a genotype-specific fashion, and we detected three unique “virus-association phenotypes,” with potential consequences for patterns of host plant use by aphid populations and crop virus epidemiology.