Dry bean (Phaseolus vulgaris L.) is an important worldwide legume crop with low to moderate levels of resistance to common bacterial blight (CBB) caused by Xanthomonas axonopodis pv. phaseoli. A total of 852 genotypes (cultivars, preliminary and advanced breeding lines) from the North Dakota State University dry bean breeding program were tested for their effectiveness as populations for genome-wide association studies (GWAS) to identify genomic regions associated with resistance to CBB, to exploit the associated markers for marker-assisted breeding (MAB), and to identify candidate genes. The genotypes were evaluated in a growth chamber for disease resistance at both the unifoliate and trifoliate stages. At the unifoliate stage, 35% of genotypes were resistant, while 25% of genotypes were resistant at the trifoliate stage. Libraries generated from each genotype were sequenced using the Illumina platform. After filtering for sequence quality, read depth, and minor allele frequency, 41,998 single-nucleotide polymorphisms (SNPs) and 30,285 SNPs were used in GWAS for the Middle American and Andean gene pools, respectively. One region near the distal end of Pv10 near the SAP6 molecular marker from the Andean gene pool explained 26.7–36.4% of the resistance variation. Three to seven regions from the Middle American gene pool contributed to 25.8–27.7% of the resistance, with the most significant peak also near the SAP6 marker. Six of the eight total regions associated with CBB resistance are likely the physical locations of quantitative trait loci identified from previous genetic studies. The two new locations associated with CBB resistance are located at Pv10:22.91–23.36 and Pv11:52.4. A lipoxgenase-1 ortholog on Pv10 emerged as a candidate gene for CBB resistance. The state of one SNP on Pv07 was associated with susceptibility. Its subsequent use in MAB would reduce the current number of lines in preliminary and advanced field yield trial by up to 14% and eliminate only susceptible genotypes. These results provide a foundational SNP data set, improve our understanding of CBB resistance in dry bean, and impact resource allocation within breeding programs as breeding populations may be used for dual purposes: cultivar development as well as genetic studies.The datasets presented in this study can be found in the NDSU repository at https://hdl.handle.net/10365/31610