SUMMARYSeptoria nodorum blotch (SNB), caused by Parastagonospora nodorum, is a disease of durum and common wheat initiated by the recognition of pathogen‐produced necrotrophic effectors (NEs) by specific wheat genes. The wheat gene Snn1 was previously cloned, and it encodes a wall‐associated kinase that directly interacts with the NE SnTox1 leading to programmed cell death and ultimately the development of SNB. Here, sequence analysis of Snn1 from 114 accessions including diploid, tetraploid, and hexaploid wheat species revealed that some wheat lines possess two copies of Snn1 (designated Snn1‐B1 and Snn1‐B2) approximately 120 kb apart. Snn1‐B2 evolved relatively recently as a paralog of Snn1‐B1, and both genes have undergone diversifying selection. Three point mutations associated with the formation of the first SnTox1‐sensitive Snn1‐B1 allele from a primitive wild wheat were identified. Four subsequent and independent SNPs, three in Snn1‐B1 and one in Snn1‐B2, converted the sensitive alleles to insensitive forms. Protein modeling indicated these four mutations could abolish Snn1–SnTox1 compatibility either through destabilization of the Snn1 protein or direct disruption of the protein–protein interaction. A high‐throughput marker was developed for the absent allele of Snn1, and it was 100% accurate at predicting SnTox1‐insensitive lines in both durum and spring wheat. Results of this study increase our understanding of the evolution, diversity, and function of Snn1‐B1 and Snn1‐B2 genes and will be useful for marker‐assisted elimination of these genes for better host resistance.