Grass carp (Ctenopharyngodon idella) is an important economic and ecological freshwater fish. Grass carp is a highly adaptive and has been introduced around the world, making it a good model to explore genomic divergence in diverse ecosystems. Habitat colonization often requires extensive adaptation to cope with environmental challenges from temperature and light variations; however, the associated genomic mechanisms underlying evolution are unclear. To evaluate the genetic diversity and selective adaptation in this species, we improved the draft genome of female grass carp using a fine genetic map and performed whole-genome resequencing to generalize genetic differentiations and variations among eight populations across its distributional range in Asia. Population structures analysis using principal component, linkage disequilibrium decay, and admixture analyses revealed that the Asian grass carp comprises two independent and genetically distinct populations, which might have resulted from geographical distributions with contrasting environments. The South Asia population exhibited reduced genetic diversity and a distinct population structure compared with those of the China and Vietnam populations. Genome selected sweep analysis revealed many diverged genomic regions containing genes enriched for the nervous system and epigenetic diversity-related genetic variation. Finally, among 27 candidate genes located in selected regions, the oxytocin gene had the highest Fst value, and is involved in parturition, social behavior, growth, and developmental processes, possibly contributing to the local adaptation of South Asia grass carp. Our results suggested that grass carp genomic divergence has been triggered and maintained by geographic isolation, revealing the genomic basis of adaptation in this species.