<p>Anthropogenic changes can drive rapid evolution in wild populations, but the role of phenotypic plasticity in such scenarios remains unclear. This uncertainty can affect applications like the design of resistance management approaches. In the case of insecticide resistance in mosquitoes, however, little is known regarding how environmental conditions, genetic variation, and their interactions jointly shape resistance phenotypes. To address this, we employed a full-sibling design to investigate the effects of larval food availability on adult broad-sense heritability and phenotypic plasticity in resistance to permethrin. Two experiments measured resistance levels in West Nile virus vectors (laboratory colony of <i>Culex pipiens</i> and two field populations of <i>Culex restuans</i>) using CDC bottle bioassays, and the time until death was tracked. Wing lengths were measured to assess if there is a relationship between body size and permethrin resistance. Based on likelihood ratio tests, the broad-sense heritability values for resistance were significant. There was substantial variance and phenotypic plasticity in both <i>Cx. restuans</i> field populations, while the laboratory colony of <i>Cx. pipiens</i> exhibited less variation. Larval food availability significantly affected resistance, but the sign of the effect varied across populations from different geographic regions, highlighting the importance of genotype by environmental interactions in this system. Our results offer valuable insights into the potential for insecticide resistance to evolve in mosquito populations and have important implications for how resistance in vectors can be assessed. We suggest changes to improve the current methodology for insecticide resistance testing and recommend that population-specific data should inform vector control schemes.</p>