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The majority of mosquito-borne illness is spread by a few mosquito species that have evolved to specialize in biting humans, yet the precise causes of this behavioral shift are poorly understood. We address this gap in the arboviral vector Aedes aegypti. We first collect and characterize the behavior of mosquitoes from 27 sites scattered across the species' ancestral range in sub-Saharan Africa, revealing previously unrecognized variation in preference for human versus animal odor. We then use modeling to show that over 80% of this variation can be predicted by two ecological factors—dry season intensity and human population density. Finally, we integrate this information with whole-genome sequence data from 375 individual mosquitoes to identify a single underlying ancestry component linked to human preference. Genetic changes associated with human specialist ancestry were concentrated in a few chromosomal regions. Our findings suggest that human-biting in this important disease vector originally evolved as a by-product of breeding in human-stored water in areas where doing so provided the only means to survive the long, hot dry season. Our model also predicts that the rapid urbanization currently taking place in Africa will drive further mosquito evolution, causing a shift toward human-biting in many large cities by 2050. • African populations of Ae. aegypti vary in preference for human versus animal odor • Preference for humans is associated with intense dry seasons and urbanization • Preference for humans has a single, shared genomic basis inside and outside Africa • Rapid urbanization could further increase human biting in many African cities by 2050 Rose et al. demonstrate that the evolution of human-biting in Aedes aegypti mosquitoes across Africa is associated with long, hot dry seasons and recent increases in human population density. This behavioral shift has a shared genomic basis inside and outside Africa; genetic changes were concentrated in key chromosomal regions. [ABSTRACT FROM AUTHOR]