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Common bean (Phaseolus vulgaris L.) is one of the most important legume crops for human consumption. The Native Seeds/SEARCH common bean collection consists of locally-adapted accessions collected from the southwestern US and northwestern Mexico. In this study, a representative panel of nearly 300 accessions from this collection was genotyped with more than 10,000 high-quality SNP markers and phenotyped for seed coat patterns. The collection consists primarily of accessions from the Mesoamerican gene pool, and they separate into three distinct subpopulations, with strong population differentiation (FST > 0.4) observed between them. Through a genome-wide association study with the Mesoamerican accessions, we identified several SNPs on chromosome 8 that are associated with seed coat pattern traits and reside proximal to the putative location of the C locus, a locus previously shown to control the pattern of the seed coat. Five myb transcription factors linked to these SNPs were identified as candidate causal genes for seed coat patterns controlled by the C locus. Furthermore, we identified a potentially novel locus on chromosome 10 that appears to control the Anasazi seed coat phenotype. Our work is the first to characterize the genetic diversity of the Native Seeds/SEARCH common bean collection, providing valuable genetic information for germplasm conservation efforts.