Drought stress is the most important environmental stress limiting maize production. ZmPTF1, a phosphate starvation-induced basic helix-loop-helix (bHLH) transcription factor (TF), contributes to root development and low-phosphate tolerance in maize. In this paper, ZmPTF1 expression, drought tolerance and the underlying mechanisms were studied by using maize ZmPTF1 overexpression lines and mutants. ZmPTF1 was found to be a positive regulator of root development, ABA synthesis, signalling pathways and drought tolerance. ZmPTF1 was also found to bind to the G-box element within the promoter of 9-cis-epoxycarotenoid dioxygenase (NCED), C-repeat-binding factor (CBF4), ATAF2/NAC081, NAC30 and other TFs and act as a positive regulator of the expression of those genes. The dramatically upregulated NCEDs led to increased ABA synthesis and activation of the ABA signalling pathway. The upregulated TFs hierarchically regulate the expression of the genes involved in root development, stress responses and modifications of transcriptional regulation. The improved root system; increased ABA content; and activated ABA-, CBF4-, ATAF2- and NAC30-mediated stress responses increased the drought tolerance of the ZmPTF1 overexpression lines, while the mutants showed opposite trends. This study describes a useful gene for transgenic breeding and helps us understand the role of a bHLH protein in plant root development and stress responses.