The hemibiotrophic fungus Apiosporina morbosa causes a deadly disease known as Black Knot (BK) in commercially cultivated Prunus domestica (European) and Prunus salicina (Japanese) plums. To explore the resistance mechanisms and disease development, plum genotypes were phenotyped for BK resistance/susceptibility by developing a BK resistance scale. Whole-genome sequencing followed by common variant analysis performed on resistant and susceptible Japanese plum genotypes revealed 52 BK resistance (R and PRR), and 31 pathogenicity-related (PR) genes with linked functional variants. Intriguingly, chromosomes 1, 4, and 6 had the highest number of R, PRR, and PR genes, and the variants associated with these genes. Among the identified putative candidate genes, XM_016791920.1 (f-box/leucine-rich repeat kinase), XM_021957420.1 (disease resistance), XM_020557425.1 (cyclic nucleotide gated ion channel), XM_020561539.1 (bactericidal protein), XM_008228053.2 (ankyrin-1-like protein), XM_008241686.2 (proline rich extension like protein), and XM_021961744.1 (leucine-rich repeat kinase) had the highest rate of variations, indicating their strong involvement in conferring BK disease resistance. Besides, the phytohormonal analysis suggested auxin-cytokinins interplay driven by A. morbosa appeared to be vital in disease progression. The fungus hampers the plant defense system via perturbance in salicylic acid (SA), jasmonic acid (JA), and gibberellic acid. In addition, our results suggest that the relationship between SA and JA in plant defense is not always antagonistic. Taken together, these findings suggest that the auxin and tryptophan profile could potentially be utilized as a biomarker for BK resistance in plums. In addition, the results of our study provide a basis for further exploration of BK resistance in Japanese and European plums.