Lateral roots (LRs) branching is crucial for water and nutrient acquisition in plants, thus determining the overall plant performance and productivity. However, the transcriptional regulation of LR development in crops and its role in enhancing stress resilience remain largely unexplored. Leveraging integrated transcriptome-wide association studies (TWAS) and single-cell RNA sequencing (scRNA-seq), we reported a basic leucine zipper (bZIP) transcription factor ZmbZIP89 as an important regulator of LRs elongation and mapped its spatial expression pattern in cortex/epidermis cell types. ZmbZIP89 activates the expression of ZmPRX47 to regulate the production of root reactive oxygen species (ROS) homeostasis, contributing to increased lateral root length (LRL) and enhanced drought resistance. Natural variations in the 3′UTR of ZmbZIP89 enhance its expression by increasing mRNA stability, leading to improved LRL and drought tolerance. These findings contribute to our understanding of the molecular mechanisms involved in lateral root development and provide potential targets for breeding stress-resilient crops.