Abstract Access to broad genomic resources and closely linked marker‐trait associations for common beans ( Phaseolus vulgaris L.) can facilitate development of improved varieties with increased yield, improved market quality traits, and enhanced disease resistance. The emergence of virulent races of anthracnose (caused by Colletotrichum lindemuthianum ) and bean common mosaic virus (BCMV) highlight the need for improved methods to identify and incorporate pan‐genomic variation in breeding for disease resistance. We sequenced the P. vulgaris Andean Diversity Panel (ADP) and performed a genome‐wide association study (GWAS) to identify associations for resistance to BCMV and eight races of anthracnose. Historical single nucleotide polymorphism (SNP)‐chip and phenotypic data enabled a three‐way comparison between SNP‐chip, reference‐based whole genome shotgun sequence (WGS)‐SNP, and reference‐free k ‐mer (short nucleotide subsequence) GWAS. Across all traits, there was excellent concordance between SNP‐chip, WGS‐SNP, and k ‐mer GWAS results—albeit at a much higher marker resolution for the WGS data sets. Significant k‐mer haplotype variation revealed selection of the linked I ‐gene and Co‐u traits in North American breeding lines and cultivars. Due to structural variation, only 9.1 to 47.3% of the significantly associated k ‐mers could be mapped to the reference genome. Thus, to determine the genetic context of cis ‐associated k ‐mers, we generated draft whole genome assemblies of four ADP accessions and identified an expanded local repertoire of disease resistance genes associated with resistance to anthracnose and BCMV. With access to variant data in the context of a pan‐genome, high resolution mapping of agronomic traits for common bean is now feasible.