Most cultivated potato () varieties are highly susceptible to common scab (). The disease is widespread in all major potato production areas and leads to high economic losses and food waste. Varietal resistance is seen as the most viable and sustainable long-term management strategy. However, resistant potato varieties are scarce, and their genetic architecture and resistance mechanisms are poorly understood. Moreover, diploid potato relatives to commercial potatoes remain to be fully explored. In the current study, a panel of 384 ethyl methane sulfonate (EMS)-mutagenized diploid potato clones were evaluated for common scab coverage, severity, and incidence traits under field conditions, and genome-wide association studies (GWASs) were conducted to dissect the genetic architecture of their traits. Using the GAPIT-MLM and RTM-GWAS statistical models, and Mann-Whitney non-parametric -tests, we show that 58 QTNs/QTLs distributed on all 12 potato chromosomes were associated with common scab resistance, 52 of which had significant allelic effects on the three traits. In total, 38 of the 52 favorable QTNs/QTLs were found to be pleiotropic on at least two of the traits, while 14 were unique to a single trait and were found distributed over 3 chromosomes. The identified QTNs/QTLs showed low to high effects, highlighting the quantitative and multigenic inheritance of common scab resistance. The QTLs/QTNs associated with the three common scab traits were found to be co-located in genomic regions carrying 79 candidate genes playing roles in plant defense, cell wall component biosynthesis and modification, plant-pathogen interactions, and hormone signaling. A total of 61 potato clones were found to be tolerant or resistant to common scab. Taken together, the data show that the studied germplasm panel, the identified QTNs/QTLs, and the candidate genes are prime genetic resources for breeders and biologists in breeding and targeted gene editing.