Understanding the genetic basis of adaptive evolution following habitat expansion can have important implications for pest management. The pink stem borer (PSB), Sesamia inferens (Walker), is a destructive pest of rice that was historically restricted to regions south of N34° latitude in China. However, with changes in global climate and farming practices, the distribution of this moth has progressively exceeded its traditional limit of 34° N and encompassed most regions in North China. However, the evolutionary processes and local adaptative changes of this species, are not yet fully understood. Here, we employed genome resequencing to genotype over 1 million of high‐quality SNPs and 20,000 SVs from 14 geographical populations across China. Three highly differentiated genetic groups were formed, corresponding to Northern and Southern China regions and the Yunnan-Guizhou Plateau. The pairwise genetic distance between locations was highly correlated with geographic and environmental distance. Our estimates of evolutionary history indicate asymmetric migration with varying population sizes across three genetic groups. Selective sweep analyses highlight the strongly selected insect cuticle GRP genes enhanced desiccation adaptability of the northern group and SETMAR gene associated with range expansion and local adaptation in the Shandong population. Based on an integrated analysis of transcriptome and enGWAS, we also identified the CYP321A7 gene as being involved in the PSB adaption to desiccation climates. Our findings revealed the phylogeography, demographic dynamics and evolutionary forces of PSB and identified potential candidate genes to explore the genetic adaptation to novel environments, which have significant implications for the development of effective strategies to control this pest.