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Flag leaf serves as an essential source of assimilates during grain filling, thereby contributing to grain yield up to 48%. Thus, high‐throughput phenotyping of flag leaves is crucial to determine their physiological and genetic basis of yield formation and drought adaptation. Here, we utilized 200 wheat cultivars to identify drought‐adaptive loci underlying candidate genes associated with flag leaf biomass and photosynthesis‐related traits using a genome‐wide association study (GWAS). GWAS revealed 21 significant marker‐trait associations for key photosynthetic traits in response to drought stress. Analysis of linkage disequilibrium (LD) in these SNPs intervals discovered 103 significant SNPs that established distinct LD blocks containing a total of 382 candidate genes putatively involved in physiological processes, including photosynthesis and water responses. Further, in silico transcript analysis identified two candidate genes in locus AX‐580365925 on chromosome 4B, those were found to be highly expressed under drought and associated with proton‐transporting ATP synthase activity and stress response pathways. Accordingly, we identified significant allelic haplotype differences on this same locus. The tolerant haplotype (higher chlorophyll content under drought) representing major allele was more abundant and stably increased photosynthetic efficiency and yield under drought scenarios. Collectively, this study offers new adaptive loci and beneficial alleles to reshape the flag leaf physiological and associated photosynthetic components for better yield and sustainability to water‐deficit stress. [ABSTRACT FROM AUTHOR]