Bean common mosaic virus (BCMV) and bean common mosaic necrosis virus (BCMNV) have a damaging impact on global common bean (Phaseolus vulgaris L.) cultivation, causing potential yield losses of over 80%. The primary strategy for controlling these viruses is through host plant resistance. This research aimed to identify and validate structural variations for the bc-ud gene as revealed by long-read sequencing, develop an efficient DNA marker to assist selection of bc-ud in snap and dry beans, and examine the interactions between the bc-ud allele and other BCMV resistance genes. A gene (Phvul.005G125100) model on chromosome Pv05, encoding a vacuolar protein-sorting 4 (Vps4) AAA+ ATPase endosomal sorting complexes required for transport (ESCRT) protein, was identified as the best candidate gene for bc-ud. An 84-bp repetitive insertion variant within the gene, exhibited 100% co-segregation with the bc-ud resistance allele across 264 common bean accessions. The 84-bp repetitive insertion was labeled with an indel marker IND_05_36225873 which was useful for tracking the bc-ud allele across diverse germplasm. A different single nucleotide polymorphism variant within the same candidate gene was associated with the bc-4 gene. Segregation in F2 populations confirmed bc-ud and bc-4 were alleles, so bc-4 was renamed bc-ur to fit gene nomenclature guidelines. The interactions of bc-ud and bc-ur with other resistance genes, such as bc-1 (receptor-like kinase on Pv03) and bc-2 (Vps4 AAA+ ATPase ESCRT protein on Pv11), validated gene combinations in the differential "host groups" effective against specific BCMV/BCMNV "pathogroups." These findings increase our understanding of the Bc-u locus, and enhance our ability to develop more resilient bean varieties through marker-assisted selection, reducing the impact of BCMV and BCMNV.