Blister blight, caused by Exobasidium vexans Massee, is a serious tea disease and leads to massive damage to tea yield and quality. WRKY transcription factors play an important role in the regulation of biotic stresses. However, the biological and molecular functions of these transcription factors during blister blight in tea plants are not known. The present study isolated a disease resistance gene, CsWRKY14, from leaves of Camellia sinensis and analysed this gene using bioinformatics. The results demonstrated that CsWRKY14 comprised multiple cis-acting elements and involved in salicylic acid (SA) signal transduction pathway. Moreover, the CsWRKY14 protein belongs to the IIe subgroup of the WRKY family located in the nucleus. The expression of CsWRKY14 was more upregulated in the resistant cultivar ‘Zhongcha 108’ (ZC) compared to the susceptible cultivar ‘Longjing changye’ (LJ). Consistently, the endogenous levels of SA and the expression of SA signaling pathway-related genes (NPR1, PR1, PR2, and PR4) were higher in ZC than in LJ, which suggests that CsWRKY14 contributes to the increase of SA concentration and activates the expression level of SA-induced pathogen-associated genes. Histochemical analysis and enzymatic activity assay revealed that the resistant cultivar ZC exhibited less H2O2 accumulation and higher activities of antioxidant enzymes. CsWRKY14-silenced plants were more sensitive to E. vexans than wild plants and exhibited a decrease in the expression of SA pathway-related genes and the antioxidant enzyme activities. Our results suggest CsWRKY14 can be used as an effective genetic resource for tea breeding against blister blight.