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<i>Megalurothrips usitatus</i> (Bagnall) is a destructive pest of legumes, such as cowpea. The biology, population dynamics and control strategies of this pest have been well studied. However, the lack of a high-quality reference genome for <i>M. usitatus</i> has hindered the understanding of key biological questions, such as the mechanism of adaptation to feed preferentially on high-protein host plants and the resistance to proteinase inhibitors (PIs). In this study, we generated a high-resolution chromosome-level reference genome assembly (247.82 Mb, 16 chromosomes) of <i>M. usitatus</i> by combining Oxford Nanopore Technologies (ONT) and Hi-C sequencing. The genome assembly showed higher proportions of GC and repeat content compared to other Thripinae species. Genome annotation revealed 18,624 protein-coding genes, including 4613 paralogs that were preferentially located in TE-rich regions. GO and KEGG enrichment analyses of the paralogs revealed significant enrichment in digestion-related genes. Genome-wide identification uncovered 506 putative digestion-related enzymes; of those, proteases, especially their subgroup serine proteases (SPs), are significantly enriched in paralogs. We hypothesized that the diversity and expansion of the digestion-related genes, especially SPs, could be driven by mobile elements (TEs), which promote the adaptive evolution of <i>M. usitatus</i> to high-protein host plants with high serine protease inhibitors (SPIs). The current study provides a valuable genomic resource for understanding the genetic variation among different pest species adapting to different plant hosts.