As an effective biological control agent,Propylea japonica (Coleoptera: Coccinellidae) preys on aphids, whiteflies, planthoppers, and small caterpillars, playing a crucial role in pest management within agro-ecological systems. However, the lack of population genomic data has hindered efforts to optimize its use in biological control. We anayzed resequencing data from 166 genomes across 29 populations spanning P. japonica’s distribution in China. This study reconstructed the species’ evolutionary history, assessed population genetic diversity and demographic structure, identified the key environmental factors driving adaptive evolution. Meanwhile, we predicted its suitable habitats across different periods using ecological niche modelling methods. The results indicated that North China (G1, Yellow River Basin) was the likely geographic origin of P. japonica. Northern and southern populations show significant genetic differentiation, with adaptive evolution in the south being the major driver. We identified genomic signatures of selection in adaptive genes associated with increased pesticide resistance and thermal tolerance. Over the past 20,000 years, effective population size of P. japonica experienced an early bottleneck during the Last Glacial Maximum period, and a subsequent rapid expansion. These insights are critical for improving the conservation and application of natural enemies, ultimately enhancing biological control in agricultural systems.