Introgression between genetically distinct populations generates variation that may promote adaptation to diverse environmental conditions. In the mosquito Aedes aegypti, the forest-associated subspecies Aedes aegypti formosus (Aaf) underwent a domestication process approximately 5000 years ago, giving rise to the globally invasive, human-associated arbovirus vector Aedes aegypti aegypti (Aaa). Despite extensive human-mediated transport, the two subspecies remain largely distinct, with admixture documented mainly in coastal Africa and Saudi Arabia. We examined Saudi Arabian Ae. aegypti across climatically contrasting regions - the humid south and arid west- using a Saudi Arabian dataset (11,939 SNPs) to examine within-country genetic and environmental variation and a global dataset (13,455 SNPs) to assess ancestry and admixture in a worldwide context. Genomic analyses revealed strong west-south differentiation, with Jazan Highland showing admixture between subspecies and the highest proportion of Aaf ancestry. Multiple pulses of gene flow into and within southern Saudi Arabia suggest Aaf populations act as a reservoir of genetic variation. Genome-wide scans identified a candidate region associated with the humidity gradient, harbouring an elongase of very long-chain fatty acids (AAEL024147), essential for cuticle production and minimizing water loss. Because the Saudi Arabian genetic background is predominantly the arid-adapted subspecies Aaa, the presence of Aaf ancestry at this locus may reflect localized introgression with adaptive relevance under an increasingly humid environment. Our findings highlight how secondary contact between divergent lineages may contribute to local adaptation in Ae. aegypti, with implications for predicting responses to environmental change.