Root system architecture (RSA) plays a vital role in plant adaptation and productivity under water‐deficit environments. In this study, we use two maize inbreeds to investigate root phenotypic and early transcriptional responses to water‐deficit stress. As evidenced by improved survival rate and photosynthetic efficiency at early seedling and late vegetative stage, CIMBL55 was characterized as a tolerant genotype versus sensitive SHEN5003. Image‐based root phenotyping revealed that drought tolerant cultivar had notably different RSA features from drought sensitive cultivar including larger root size, longer root length, and more number of lateral roots and seminal roots. Dynamic transcriptome investigations on primary and seminal root integrating differential gene expression, temporal gene co‐expression, and weighted gene co‐expression network analysis (WGCNA) revealed a high degree of genotype‐ and root type‐specificity in response to PEG‐induced water deficit. The higher drought tolerability of CIMBL55 versus SHEN5003 can be attributed to the enhanced expression of genes associated with antioxidant defense and a higher proportion of water‐deficit responsive genes. Upon water deficit, seminal roots exhibited more dramatic transcriptional changes than the primary root, and a more exclusive functional association with stress response. Genome‐wide WGCNA identified system‐level functionality of genes associated with specific root traits. Multiple root‐specific and root‐predominant hub genes were identified with functions involved in transcriptional regulation, root development, and drought response. Conclusively, integrated root phenotypic and transcriptomic analyses identified important root system architectures and water‐deficit responsive gene networks in maize. Findings will serve a valuable resource that merits in‐depth functional analyses toward a better understanding of RSA‐associated drought tolerance in maize.