Apple blotch (AB) is an emerging disease in apple production, primarily causing premature defoliation. The rise of orchard management practices reducing fungicide use has coincided with an increase in AB incidence in Europe. Breeding for resistance to AB became important for long-term disease management. Depending on the genetic complexity of the trait, breeding can be supported using either marker-assisted or genomic selection. However, no such tools are currently available for AB. To address this issue, we established two biparental mapping populations, ‘Topaz’ × ‘Granny Smith’ and ‘Topaz’ × ‘Parkapfel’, and a diversity panel of 122 genotypes, all evaluated for their resistance to AB under natural field conditions across three growing seasons. Quantitative trait locus (QTL) mapping identified five associated loci on chromosomes 3, 5, 6, 10, and 11, each explaining a maximum of 12% of phenotypic variance, indicating a polygenic architecture of AB resistance. Strong seasonal effects were observed in disease development, and they were either removed (G model) or explicitly modeled (G+G×E model) using genomic prediction approaches. The average predictive ability reached 0.47 for the G model and 0.38 for the G+G×E model. While the detected QTLs have small individual effects that constrain their use in marker-assisted selection, the moderate predictive ability of genomic prediction models demonstrates the potential of genomic selection for accelerating resistance breeding. These findings provide the first genomic tools to support breeding for resistance to AB and illustrate the utility of genome-wide approaches in managing complex traits.