Powdery mildew caused by Blumeria graminis f.sp. tritici (Bgt) is a detrimental disease of bread wheat (Triticum aestivum). Bgt infection initiates with the germination of its conidia, which is stimulated by plant cuticle-derived wax signals. Here, we identified wheat 3-KETOACYL-CoA SYNTHASE (TaKCS6), a homolog of barley HvKCS6, as a key enzyme in the biosynthesis of wheat cuticular wax. We found that both cuticular wax accumulation and Bgt germination were impeded on leaves of TaKCS6-knockdown plants. The TaKCS6 promoter-associated bHLH type transcription factor 1 (TaKPAB1) binds to the TaKCS6 promoters and recruits the CHD3 protein TaCHR729 to them via physical association. Knockdown of TaCHR729 results in decreased trimethylation of histone H3 Lys 4 (H3K4me3) at the TaKCS6 promoters and down-regulation of TaKCS6 transcription, leading to a reduction of cuticular wax accumulation and Bgt germination on leaves. We further identified very-long-chain aldehydes with a chain length above C24 as the signals regulated by the TaCHR729-TaKPAB1-TaKCS6 pathway for stimulating Bgt germination. Our study thus reveals that the transcription factor-mediated recruitment of chromatin remodeling machinery is essential for regulating the biosynthesis of cuticular wax that is required for stimulating Bgt germination in bread wheat.