Abstract Background Sooty mold (SM) disease severely threatens tea plant health, reducing yield and quality. Driven by climate change and intensive farming practices, SM prevalence in China has surged, causing significant economic losses and forcing farmers to rely on chemical fungicides, which compromise environmental sustainability. Despite its impact, the molecular mechanisms underlying tea plant defenses against SM remain unclear. Results Integrated transcriptomic, sRNAome, and degradome analyses revealed that differentially expressed genes (DEGs) exhibited infection-level-dependent expression patterns. Post-transcriptional regulation by miRNAs was identified through sRNAome-degradome mapping, with six miRNA-target defense pairs validated by 5′ RLM-RACE and qRT-PCR. Co-expression network analysis showed that two miRNA-target pairs, PC-5p-33681_128-auxin response factor (CsARF) and ppe-MIR535b-p3-1ss12TC-aldehyde dehydrogenase (CsALDH), play crucial roles in responding to SM infection. Furthermore, 5′ RLM-RACE and dual-luciferase assays revealed that the PC-5p-33681_128 and ppe-MIR535b-p3-1ss12TC could regulate the expression of CsARF and CsALDH by mRNA cleavage, respectively. Conclusion This study elucidates miRNA-mediated defense networks in tea plants against SM, offering actionable targets for breeding SM-resistant cultivars via genetic engineering or marker-assisted selection. Implementing these strategies could reduce yield losses, stabilize farmer incomes, and minimize environmental harm from fungicide overuse. This work advances climate-resilient practices for the global tea industry by linking molecular insights to sustainable agriculture.