Understanding the genetic basis of traits of economic importance under drought stressed and well-watered conditions is important in enhancing genetic gains in dry beans (Phaseolus vulgarisL.). This research aims to: (i) identify markers associated with agronomic and physiological traits for drought tolerance and (ii) identify drought-related putative candidate genes within the mapped genomic regions. An andean and middle-american diversity panel (AMDP) comprising of 185 genotypes was screened in the field under drought stressed and well-watered conditions for two successive seasons. Agronomic and physiological traits,viz., days to 50% flowering (DFW), plant height (PH), days to physiological maturity (DPM), grain yield (GYD), 100-seed weight (SW), leaf temperature (LT), leaf chlorophyll content (LCC) and stomatal conductance (SC) were phenotyped. Principal component and association analysis were conducted using the filtered 9370 Diversity Arrays Technology sequencing (DArTseq) markers. The mean PH, GYD, SW, DPM, LCC and SC of the panel was reduced by 12.1, 29.6, 10.3, 12.6, 28.5 and 62.0%, respectively under drought stressed conditions. Population structure analysis revealed two sub-populations, which corresponded to the andean and middle-american gene pools. Markers explained 0.08–0.10, 0.22–0.23, 0.29–0.32, 0.43–0.44, 0.65–0.66 and 0.69–0.70 of the total phenotypic variability (R2) for SC, LT, PH, GYD, SW and DFW, respectively under drought stressed conditions. For well-watered conditions,R2varied from 0.08 (LT) to 0.70 (DPM). Overall, 68 significant (p < 10−03) marker-trait associations (MTAs) and 22 putative candidate genes were identified across drought stressed and well-watered conditions. Most of the identified genes had known biological functions related to regulating the response to drought stress. The findings provide new insights into the genetic architecture of drought stress tolerance in common bean. The findings also provide potential candidate SNPs and putative genes that can be utilized in gene discovery and marker-assisted breeding for drought tolerance after validation.