Grapevine powdery mildew (GPM), caused by Erysiphe necator, poses a significant threat to all green grapevine tissues, leading to substantial economic losses in viticulture. Traditional grapevine cultivars derived from Vitis vinifera are highly susceptible to GPM, whereas the wild Chinese accession Baishui-40 (BS-40) of V. piasezkii var. pagnucii exhibits robust resistance. To illuminate the genetic basis of resistance, we sequenced and assembled the chromosome-level genome of ‘BS-40’, achieving a total mapped length of 578.6 Mb distributed across nineteen chromosomes. A comprehensive annotation identified 897 nucleotide-binding leucine-rich repeat (NLR) genes in the ‘BS-40’ genome, which exhibited high sequence similarity across Vitis genomes. 284 of these NLR genes were differentially expressed upon GPM infection. A hybrid population of ‘BS-40’ and V. vinifera was constructed and 195 progenies were whole-genome re-sequenced. A new GPM-resistant locus, designated Ren17, located within the 0.74–1.23 Mb region on chromosome 1 was identified using genome-wide association study, population selection, and QTL analysis. Recombinant events indicated that an NLR gene cluster between 1 045 489 and 1 089 719 bp on chromosome 1 is possibly the key contributor to GPM resistance in ‘BS-40’. Based on an SNP within this region, a dCAPS marker was developed that can predict the GPM resistance in ‘BS-40’-derived materials with 99.4% accuracy in the progenies of ‘BS-40’ and V. vinifera. This chromosome-level genome assembly of V. piasezkii var. pagnucii provides a valuable resource not only for grapevine evolution, genetic analysis, and pan-genome studies but also a new locus Ren17 as a promising target for GPM-resistant breeding in grapevine.

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