Interactions and co-evolution between plants and herbivorous insects are critically important in agriculture. Brown planthopper (BPH) is the most severe insect of rice, and the biotypes adapt to feed on different rice genotypes. Here, we present genomics analyses on 1,520 global rice germplasms for resistance to three BPH bi-otypes. Genome-wide association studies iden-tified 3,502 single nucleotide polymorphisms (SNPs) and 59 loci associated with BPH resist-ance in rice. We cloned a previously unidentified gene Bph37 that confers resistance to BPH. The associated loci showed high nucleotide di-versity. Genome-wide scans for trans-species polymorphisms revealed ancient balancing se-lection at the loci. The secondarily evolved insect biotypes Ⅱ and Ⅲ exhibited significantly higher virulence and overcame more rice varieties than the primary biotype Ⅰ. In response, more SNPs and loci evolved in rice for resistance to biotypes Ⅱ and Ⅲ. Notably, three exceptional large regions with high SNP density and resistance-associated loci on chromosomes 4 and 6 appear distinct between the resistant and susceptible rice vari-eties. Surprisingly, these regions in resistant rice might have been retained from wild species Oryza nivara. Our findings expand the under-standing of long-term interactions between rice and BPH and provide resistance genes and germplasm resources for breeding durable BPH-resistant rice varieties.