A subspecies of the mosquito Aedes aegypti recently evolved to specialize on human hosts—preferring human odor over non-human animal odor and living alongside humans rather than in forests like its ancestors. Here, we report on how this anthropophilic specialist has evolved to thrive in habitats near humans. We find that derived domestic (Ae. aegypti aegytpi) mosquito larvae hatch readily in oxygen-rich water, while ancestral Ae. aegypti formosus require deoxygenated water. Using genetic crosses, we demonstrate this behavioral difference is heritable, and decompose the genetic basis into a maternal effect that persists across conditions, as well as a zygotic effect present only in oxygen-rich water (i.e., GxE). Our findings—revealing an interaction between genotype and oxygen sensation—therefore point to specific molecules and neurons in controlling this evolved behavioral difference. We next examine the ecology of mosquito breeding sites including unmanipulated natural sites and experimental containers. We find that while ancestral-type sites such as tree holes are consistently low in dissolved oxygen (DO), domestic sites are highly variable and often have high DO levels. Thus, there is a concordance between each subspecies’ hatching behavior and the aquatic habitats available to it in the wild. Our results suggest the derived domestic form may have diverged from ancestral behavior to exploit breeding sites provided by humans. Hatching behavior presents an opportunity to study the genetic and neural underpinnings of behavioral evolution, and to better understand how animals adapt to built environments in the Anthropocene.