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Summary: Stomatal density (SD) is closely related to crop drought resistance. Understanding the genetic basis for natural variation in SD may facilitate efforts to improve water‐use efficiency. Here, we report a genome‐wide association study for SD in maize seedlings, which identified 18 genetic variants that could be resolved to seven candidate genes. A 3‐bp insertion variant (InDel1089) in the last exon of Zea mays (Zm) IRX15A (Irregular xylem 15A) had the most significant association with SD and modulated the translation of ZmIRX15A mRNA by affecting its secondary structure. Dysfunction of ZmIRX15A increased SD, leading to an increase in the transpiration rate and CO2 assimilation efficiency. ZmIRX15A encodes a xylan deposition enzyme and its disruption significantly decreased xylan abundance in secondary cell wall composition. Transcriptome analysis revealed a substantial alteration of the expression of genes involved in stomatal complex morphogenesis and drought response in the loss‐of‐function of ZmIRX15A mutant. Overall, our study provides important genetic insights into the natural variation of leaf SD in maize, and the identified loci or genes can serve as direct targets for enhancing drought resistance in molecular‐assisted maize breeding. [ABSTRACT FROM AUTHOR]