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Malaria in South America remains a serious public health problem. () is the most important malaria vector across tropical Latin America. Vector-targeted disease control efforts require a thorough understanding of mosquito demographic and evolutionary patterns. We present and analyze whole genomes of 1094 (median depth 18x) from six South American countries. We observe deep geographic population structure, high genetic diversity including thirteen putative segregating inversions, and no evidence for cryptic sympatric taxa despite high interpopulation divergence. Strong signals of selection are plausibly driven by insecticides, especially on cytochrome P450 genes, one of which we validated experimentally. Our results will facilitate effective mosquito surveillance and control, while highlighting ongoing challenges that a diverse vector poses for malaria elimination in the western hemisphere.