Some of the major impacts of climate change are expected in the poorest regions of the world where drought stress and nutrient deficiency are already a main issue. Legumes are an essential food crop for the poorest because of their high dietary protein and micronutrient contents. However, they are generally drought susceptible. Therefore, our goal in this study was to explore allele diversity at abiotic stress responsive candidate genes in the only drought tolerant cultivated bean species of the genus Phaseolus, tepary bean (P. acutifolius A. Gray) and its related species P. parvifolius Freytag. Specifically, we estimated drought tolerance in 52 tepary bean s.l. geo-referenced germplasm accessions from the P. acutifolius–parvifolius clade using climate information, and used this estimated drought stress index to examine allele correlations with Asr2, Dreb2B and ERECTA-encoding candidate genes for drought tolerance. Genetic clustering showed that cultivated and wild P. acutifolius were intermingled with P. acutifolius var. tenuifolius and P. parvifolius, signifying that allele diversity at candidate genes for drought tolerance was not scarce in tepary bean s.l. Dreb2B and ERECTA-encoding genes harbored signatures of directional/purifying selection, likely in favor of adaptive alleles selectively advantageous because each had two SNPs significantly correlated (p-value < 0.05) with habitat drought stress at six and 12 months. These results suggest that tepary bean s.l. is a reservoir of novel alleles at candidate genes for drought tolerance, as expected for a drought-tolerant species that originated in warmer and arid environments. Abiotic stress responsive candidate genes also exhibit comparable patterns of selective signatures when comparing orthologous across species, which speaks for a predominant role of gene sub-functionalization likely due to ecological constrains. Our study therefore corroborates that the candidate gene approach is still an effective alternative for marker validation across a broader genetic basis of germplasm accessions. Further efforts to determine the genetic architecture of drought tolerance will unlock novel alleles hidden in a crop with limited modern relevance as tepary bean, but capable of acting as a donor in backcrossing and genome editing strategies with elite common bean lines aiming to meet the imminent demands of a drier world.