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Brown planthopper (BPH), one of the most important pests of the rice (Oryza sativa) crop, becomes catastrophic under severe infestations and causes up to 60% yield loss. The highly disastrous BPH biotype in the Indian sub-continent is Biotype 4, which also known as the South Asian Biotype. Though many resistance genes were mapped until now, the utility of the resistance genes in the breeding programs is limited due to the breakdown of resistance and emergence of new biotypes. Hence, to identify the resistance genes for this economically important pest, we have used a multi-parent advanced generation intercross (MAGIC) panel consisting of 391 lines developed from eight indica founder parents. The panel was phenotyped at the controlled conditions for two consecutive years. A set of 27,041 cured polymorphic single nucleotide polymorphism (SNPs) and across-year phenotypic data were used for the identification of marker–trait associations. Genome-wide association analysis was performed to find out consistent associations by employing four single and two multi-locus models. Sixty-one SNPs were consistently detected by all six models. A set of 190 significant marker-associations identified by fixed and random model circulating probability unification (FarmCPU) were considered for searching resistance candidate genes. The highest number of annotated genes were found in chromosome 6 followed by 5 and 1. Ninety-two annotated genes identified across chromosomes of which 13 genes are associated BPH resistance including NB-ARC (nucleotide binding in APAF-1, R gene products, and CED-4) domain-containing protein, NHL repeat-containing protein, LRR containing protein, and WRKY70. The significant SNPs and resistant lines identified from our study could be used for an accelerated breeding program to develop new BPH resistant cultivars.