Alternaria blotch, a major apple (Malus × domestica Borkh.) fungal disease in Japan, is caused by the Alternaria alternata apple pathotype that produces a host-selective toxin called AM-toxin. Although control of Alternaria blotch currently relies on spring-to-summer fungicide use, there is a growing need for sustainable agriculture practices that reduce chemical inputs in orchards. Therefore, breeding cultivars for resistance to Alternaria blotch is of particular interest. Given that ‘Golden Delicious’ (GD) and several of its offspring cultivars are moderately susceptible to the disease, a genetic analysis of their susceptibility was performed. Quantitative trait locus (QTL) analysis of the ‘Fuji’ × ‘GD’ population identified a single QTL on chromosome 11 in ‘GD’, which explained 48.7% of the phenotypic variation. This QTL was located in the same region as the previously identified susceptibility gene Alt derived from ‘Starking Delicious’. Therefore, we named it QTL Alt2, a putative allele of Alt (later renamed Alt1). Interaction analysis revealed that Alt1 was dominant over Alt2. A DNA marker set that simultaneously detects Alt1 and Alt2 was developed for breeding use. This marker shed light on the inheritance of the Alt locus in modern Japanese cultivars and selections. Moreover, Alt2 was less common than Alt1 in heirloom cultivars. These findings offer new insights into apple breeding for Alternaria blotch resistance and the interaction mechanism between apple and host-selective toxin-producing A. alternata.