Cultivated potato (Solanum tuberosum) is known to be highly susceptible to drought. With climate change and its frequent episodes of drought, potato growers will face increased challenges to achieving their yield goals. Currently, a high proportion of untapped potato germplasm remains within the diploid potato relatives, and the genetic architecture of the drought tolerance and maturity traits of diploid potatoes is still unknown. As such, a panel of 384 ethyl methanesulfonate-mutagenized diploid potato clones were evaluated for drought tolerance and plant maturity under field conditions. Genome-wide association studies (GWAS) were conducted to dissect the genetic architecture of the traits. The results obtained from the genetic structure analysis of the panel showed five main groups and seven subgroups. Using the Genome Association and Prediction Integrated Tool-mixed linear model GWAS statistical model, 34 and 17 significant quantitative trait nucleotides (QTNs) were found associated with maturity and drought traits, respectively. Chromosome 5 carried most of the QTNs, some of which were also detected by using the restricted two-stage multi-locus multi-allele-GWAS haploblock-based model, and two QTNs were found to be pleiotropic for both maturity and drought traits. Using the non-parametric U-test, one and three QTNs, with 5.13%-7.4% phenotypic variations explained, showed favorable allelic effects that increase the maturity and drought trait values. The quantitaive trait loci (QTLs)/QTNs associated with maturity and drought trait were found co-located in narrow (0.5-1 kb) genomic regions with 56 candidate genes playing roles in plant development and senescence and in abiotic stress responses. A total of 127 potato clones were found to be late maturing and tolerant to drought, while nine were early to moderate-late maturing and tolerant to drought. Taken together, the data show that the studied germplasm panel and the identified candidate genes are prime genetic resources for breeders and biologists in conventional breeding and targeted gene editing as climate adaptation tools.