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Animals can modulate their own exposure to environmental contaminants through behavioral plasticity such as diet and habitat choice. However, it remains unclear if behavior also has cascading effects on contaminant exposure across multiple generations. In insects, oviposition site selection is an important behavior females can use to modify offspring contaminant exposure risk. In this study, we use the yellow fever mosquito, Aedes aegypti, to test how methylmercury (MeHg) affects oviposition site selection. We found that mosquito larval development rate and survival were negatively affected at MeHg concentrations ≥100 ppb. Adult females not exposed to MeHg as larvae avoided oviposition sites with high MeHg concentrations (>50 ppb), but MeHg exposure at the larval stage significantly affected this oviposition site selection. Specifically, females raised from larvae exposed to non-toxic MeHg levels (i.e., five-50 ppb) showed a significant increase in preference for oviposition sites contaminated with toxic MeHg concentrations (≥500 ppb), compared to unexposed controls. This maladaptive behavioral response could be because, when conditioned with non-toxic MeHg concentrations, MeHg-associated olfactory cues act as a “supernormal” stimulus during oviposition site selection. Importantly, however, this maladaptive behavioral response is eliminated in female mosquitoes raised from larvae exposed to toxic MeHg concentrations (i.e. 100 ppb), and these mosquitoes showed a significant increase in preference for MeHg uncontaminated oviposition sites, compared to unexposed controls. Thus, in mosquitoes, the magnitude of MeHg exposure in one generation can impact MeHg exposure in subsequent generations by altering oviposition site selection behavior. Our results have broad implications for our understanding of how contaminant-mediated behavioral modifications can feedback on contaminant exposure risk across multiple generations, and consequently how behavior can affect the evolutionary trajectory of organisms inhabiting a heterogeneously contaminated environment.