Root rot in Camellia oleifera complicates the development of targeted control measures owing to its complex aetiology. Although breeding resistant varieties of C. oleifera presents a promising solution, research into cultivation strategies and potential resistance mechanisms against root rot remains limited. In this study, we investigated six cultivars of C. oleifera that exhibit varying levels of resistance to root rot. We conducted transcriptome analysis, measurements of soil physicochemical properties and an analysis of the fungal microbiome to explore the relationship between Fusarium-induced root rot and flavonoid compounds in the rhizosphere. The resistant cultivar CL18 demonstrated superior performance concerning root rot incidence, root health status and the expression levels of genes associated with flavonoid biosynthesis in this study. Significant differences were observed in the composition and diversity of rhizosphere fungal communities among the various cultivars of C. oleifera. The abundance of Fusarium in the rhizosphere soil of CL18 was low, and a negative correlation was identified between the flavonoid content in the soil and the abundance of Fusarium. Our study uncovers the role of flavonoids in the resistance of C. oleifera to root rot, thereby offering new strategies for disease management and the breeding of resistant cultivars.