Cotton cultivation is conquered by transgenic Bt upland cotton hybrids in India. Bt gene does not provide resistance against sucking insect pests. Due to the inherent vulnerability of extant Bt cotton hybrids to sap-sucking insect pests including leafhopper, upland cotton cultivation is seriously threatened by surging populations of these pests. Consistent and extensive screening of upland cotton germplasm over the years has revealed absence of adequate resistance against leafhopper. Here, we report introgression of leafhopper tolerance from a diploid A-genome cotton species, Gossypium arboreum into G. hirsutum. The dominance of leafhopper tolerance was observed over its susceptibility. Genetic analysis revealed that tolerance to leafhopper was inherited in a simple Mendelian fashion and was controlled by two genes, either singly or in combination. Using bulked segregant analysis, two simple-sequence repeat markers, namely NAU 922 and BNL 1705, located on chromosomes A5 and A11 respectively, were tagged with leafhopper tolerance. To the best of our knowledge, this is the first report of molecular tagging of leafhopper tolerance introgressed from G. arboreum into G. hirsutum. A significant negative association was observed between leaf trichome density and leafhopper nymph population.