Understanding the genetic architecture of drought stress tolerance in bread wheat at seedling and reproductive stages is crucial for developing drought-tolerant varieties. In the present study, 192 diverse wheat genotypes, a subset from the Wheat Associated Mapping Initiative (WAMI) panel, were evaluated at the seedling stage in a hydroponics system for chlorophyll content (CL), shoot length (SLT), shoot weight (SWT), root length (RLT), and root weight (RWT) under both drought and optimum conditions. Following that, a genome-wide association study (GWAS) was carried out using the phenotypic data recorded during the hydroponics experiment as well as data available from previously conducted multi-location field trials under optimal and drought stress conditions. The panel had previously been genotyped using the Infinium iSelect 90K SNP array with 26,814 polymorphic markers. Using single as well as multi-locus models, GWAS identified 94 significant marker-trait associations (MTAs) or SNPs associated with traits recorded at the seedling stage and 451 for traits recorded at the reproductive stage. The significant SNPs included several novel, significant, and promising MTAs for different traits. The average LD decay distance for the whole genome was approximately 0.48 Mbp, ranging from 0.07 Mbp (chromosome 6D) to 4.14 Mbp (chromosome 2A). Furthermore, several promising SNPs revealed significant differences among haplotypes for traits such as RLT, RWT, SLT, SWT, and GY under drought stress. Functional annotation andin silicoexpression analysis revealed important putative candidate genes underlying the identified stable genomic regions such as protein kinases, O-methyltransferases, GroES-like superfamily proteins, NAD-dependent dehydratases, etc. The findings of the present study may be useful for improving yield potential, and stability under drought stress conditions.