Development of apple (Malus domestica) cultivars resistant to fire blight, a devastating bacterial disease caused by Erwinia amylovora, is a priority for apple breeding programs. Towards this goal, the inactivation of members of the HIPM and DIPM gene families with a role in fire blight susceptibility (S genes) can help achieve sustainable tolerance. We have investigated the genomic diversity of HIPM and DIPM genes in Malus germplasm collections and used a candidate gene-based association mapping approach to identify SNPs (single nucleotide polymorphisms) with significant associations to fire blight susceptibility. A total of 87 unique SNP variants were identified in HIPM and DIPM genes across 93 Malus accessions. Thirty SNPs showed significant associations (p < 0.05) with fire blight susceptibility traits, while two of these SNPs showed highly significant (p < 0.001) associations across two different years. This research has provided knowledge about genetic diversity in fire blight S genes in diverse apple accessions and identified candidate HIPM and DIPM alleles that could be used to develop apple cultivars with decreased fire blight susceptibility via marker-assisted breeding or biotechnological approaches.