Identification of central genes governing plant drought tolerance is fundamental to molecular breeding and crop improvement. Here, maize transcription factorZmHsf28is identified as a positive regulator of plant drought responses.ZmHsf28exhibited inducible gene expression in response to drought and other abiotic stresses. Overexpression ofZmHsf28diminished drought effects in Arabidopsis and maize. Gene silencing ofZmHsf28via the technology of virus-induced gene silencing (VIGS) impaired maize drought tolerance. Overexpression ofZmHsf28increased jasmonate (JA) and abscisic acid (ABA) production in transgenic maize and Arabidopsis by more than two times compared to wild-type plants under drought conditions, while it decreased reactive oxygen species (ROS) accumulation and elevated stomatal sensitivity significantly. Transcriptomic analysis revealed extensive gene regulation byZmHsf28with upregulation of JA and ABA biosynthesis genes, ROS scavenging genes, and other drought related genes. ABA treatment promotedZmHsf28regulation of downstream target genes. Specifically, electrophoretic mobility shift assays (EMSA) and yeast one-hybrid (Y1H) assay indicated thatZmHsf28directly bound to the target gene promoters to regulate their gene expression. Taken together, our work provided new and solid evidence thatZmHsf28improves drought tolerance both in the monocot maize and the dicot Arabidopsis through the implication of JA and ABA signaling and other signaling pathways, shedding light on molecular breeding for drought tolerance in maize and other crops.