In agrosystems, pests are submitted to strong human-imposed selective pressures to which they sometimes adapt rapidly, either through selection of genotypes resulting from mutation and/or recombination events, or through phenotypic plasticity. Understanding how insects respond to such selective pressures is of great importance for sustainable pest management strategies, such as the use of resistant plants. In this study, we investigated the genetic and phenotypic variability of anholocyclic Aphis gossypii Glover (Hemiptera: Aphididae) strains, in response to the resistance gene Vat that is present in melon crops. Forty-nine aphid colonies were sampled on several melon crops in southern France, genotyped using 15 microsatellite loci, and tested in phenotypic experiments using Vat or non-Vat melons. The level of genetic polymorphism between these colonies was low, as only seven multilocus genotypes were detected. In contrast, the phenotypic variability for life-history and behavioral traits between colonies, including those sharing the same genotype, was unexpectedly high, with a continuum of response to the Vat gene from complete susceptibility to strong virulence. The low genetic polymorphism associated with a strong phenotypic variability highlights the high adaptive potential of A. gossypii and the major role of environmental cues in shaping phenotypic responses of this aphid to pest management strategies