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Abstract Understanding the genetic basis of adaptive evolution following habitat expansion can have important implications for pest management. The pink rice borer (PRB),Sesamia inferens(Walker), is a destructive pest of rice that was historically restricted to regions south of 34° N latitude in China. However, with changes in global climate and farming practices, the distribution of this moth has progressively expanded, encompassing most regions in North China. Here, 3 highly differentiated subpopulations were discovered using high‐quality single‐nucleotide polymorphism and structural variant datasets across China, corresponding to northern, southern China regions, and the Yunnan‐Guizhou Plateau, with significant patterns of isolation by geographic and environmental distances. Our estimates of evolutionary history indicate asymmetric migration with varying population sizes across the 3 subpopulations. Selective sweep analyses estimated strong selection at insect cuticle glycine‐rich cuticular protein genes which are associated with enhanced desiccation adaptability in the northern group, and at the histone‐lysine‐N‐methyltransferase gene associated with range expansion and local adaptation in the Shandong population. Our findings have significant implications for the development of effective strategies to control this pest.