Soybean is a high oil and protein-rich legume with several production constraints. Globally, several fungi, viruses, nematodes, and bacteria cause significant yield losses in soybean. Coniothyrium glycines (CG), the causal pathogen for red leaf blotch disease, is the least researched and causes severe damage to soybean. The identification of resistant soybean genotypes and mapping of genomic regions associated with resistance to CG is critical for developing improved cultivars for sustainable soybean production. This study used single nucleotide polymorphism (SNP) markers generated from a Diversity Arrays Technology (DArT) platform to conduct a genome-wide association (GWAS) analysis of resistance to CG using 279 soybean genotypes grown in three environments. A total of 6395 SNPs was used to perform the GWAS applying a multilocus model Fixed and random model Circulating Probability Unification (FarmCPU) with correction of the population structure and a statistical test p-value threshold of 5%. A total of 19 significant marker–trait associations for resistance to CG were identified on chromosomes 1, 5, 6, 9, 10, 12, 13, 15, 16, 17, 19, and 20. Approximately 113 putative genes associated with significant markers for resistance to red leaf blotch disease were identified across soybean genome. Positional candidate genes associated with significant SNP loci-encoding proteins involved in plant defense responses and that could be associated with soybean defenses against CG infection were identified. The results of this study provide valuable insight for further dissection of the genetic architecture of resistance to CG in soybean. They also highlight SNP variants and genes useful for genomics-informed selection decisions in the breeding process for improving resistance traits in soybean.