Powdery mildew, caused by the biotrophic fungal pathogen Blumeria graminis f. sp. tritici, is a major limitation for wheat yield. However, the molecular mechanisms underlying wheat resistance against powdery mildew remain largely unclear. In this study, we report the role of JASMONATE-ZIM domain protein TaJAZ1 in regulating bread wheat resistance against powdery mildew. We generated transgenic bread wheat lines over-expressing the truncated TaJAZ1 without the Jas motif, which showed increased TaPR1/2 gene expression and reactive oxygen species accumulation, leading to enhanced resistance against powdery mildew. Simultaneously, we identified a Jasmonic acid (JA)-induced bHLH transcription factor TaMYC4 in bread wheat. We demonstrated that TaJAZ1 directly interacts with TaMYC4 to repress its transcriptional activity. Meanwhile, we show that the ZIM domain of TaJAZ1 interacts with the C terminus of TaNINJA, whereas the N-terminal EAR motif of TaNINJA interacts with the transcriptional co-repressor TaTPL. Collectively, our work pinpoints TaJAZ1 as a favorable gene to enhance bread wheat resistance toward powdery mildew, and provides a molecular framework for JA signaling in bread wheat.