Drought stress threatens crop production. Despite the established significance of ethylene-responsive factors (ERFs) in plant drought stress responses, the molecular mechanisms underlying this process remain poorly understood. Here, we report that the ERF transcription factor TaERF8 pay a positive role in wheat drought tolerance. TaERF8 overexpression enhanced drought tolerance in transgenic wheat, while silencing of TaERF8 increased drought susceptibility. Further RNA sequencing analysis combined with biochemical assays revealed that TaERF8 activates the expression of proline biosynthesis genes TaP5CS1 and TaP5CR1 by binding to their promoters. Consistently, under normal and drought stress conditions, TaERF8- and TaP5CS1-overexpression lines showed higher proline accumulation compared with the wild-type. Furthermore, overexpression of TaP5CS1 significantly improved wheat drought tolerance. Moreover, interaction between TaERF8 and the bHLH transcription factor TaASK2 synergistically enhance activation towards TaP5CS1 and TaP5CR1 transcription. Overexpression of TaASK2 improved wheat drought tolerance by promoting proline accumulation. In addition, TaERF8 and TaASK2 were up-regulated by ABA and drought stress, and confirmed as the targets of ABA-responsive element binding factor 2 (TaABF2). Taken together, our findings elucidate the mechanism underlying the TaABF2-TaERF8/TaASK2-TaP5CS1/TaP5CR1 module in response to drought stress and identify candidate genes for developing elite varieties with enhanced drought tolerance in wheat.