Drought stress constitutes a major threat for the global wheat production. Identification of the genetic components underlying drought tolerance in wheat is of great importance. Through a genome-wide association study, we identified a natural allele of a zinc finger-type transcription factor TaDT1-A in chromosome 2A of wheat genome that confers drought tolerance without imposing trade-offs between tolerance and yield. This allele, named as TaDT1-AhapⅠ, causes an 899-bp deletion in the promoter of the TaDT1-A gene, which results in enhanced expression of the gene through escaping the binding of the repressive MYC transcription factor and, consequently, a promotion of stomata dynamics and water use efficiency via enhancing autophagy activity. Our discovery highlights genetic insights into the natural variation of wheat drought tolerance. The identified loci or genes can serve as direct targets for both genetic engineering and selection for wheat trait improvement.