Clubroot disease caused by Plasmodiophora brassicae is one of the most devastating diseases affecting cruciferous crops. P. brassicae is an obligate biotrophic protist that parasitizes plant roots, which limits research on this pathogen. Jasmonic acid (JA)-mediated resistance pathways play a significant role in plant resistance to clubroot. However, how P. brassicae overcomes this resistance remains unclear. In this study, an effector from P. brassicae, PBRA_006697, was identified, which is highly conserved across various isolates of P. brassicae and is highly expressed during the early stages of secondary infection. Heterologous expression of PBRA_006697 in Arabidopsis thaliana demonstrated that PBRA_006697 can inhibit the JA resistance signaling pathway while promoting the occurrence of clubroot disease. Furthermore, using yeast two-hybrid (Y2H), bimolecular fluorescence complementation (BiFC), and firefly luciferase complementation imaging assays, PBRA_006697 was found to interact with the A. thaliana B-BOX transcription factor BBX24. Subsequent studies demonstrated that PBRA_006697 can destabilize BBX24 via the 26S proteasome degradation pathway. Finally, the incidence of clubroot disease and the JA signaling pathway in bbx24 mutants and overexpression lines were examined, revealing that BBX24 positively regulates the JA signaling pathway and the resistance of A. thaliana to clubroot. In summary, this study reveals a novel mechanism by which P. brassicae inhibits plant immunity, thereby enriching our understanding of its pathogenic mechanisms.