The interaction between Plasmodiophora brassicae and Arabidopsis thaliana reveals a complex struggle for cellular control, with HSP70 proteins playing a pivotal role. We demonstrate that Plasmodiophora infection induces HSP70 accumulation in Arabidopsis roots, and mutations in specific HSP70 isoforms either promote (HSP70-1, HSP70-13, HSP70-14) or suppress (HSP70-5, HSP70-12) the onset of clubroot disease. Analysis of mutant lines revealed that mutations in HSP70 trigger compensatory accumulation of other isoforms, underscoring the dynamic regulation of the chaperone network. Proteomic profiling of root galls during infection showed strong correlations between pathogen load and the abundance of Plasmodiophora HSP70 protein CEO96729. Interactomics analyses revealed that CEO96729 interacts with host proteins involved in Plasmodiophora responses, including extracellular GDSL esterase/lipase, and forms heterodimers with host HSP70 isoforms. These findings suggest that Plasmodiophora hijacks the host's chaperone machinery to facilitate its infection, offering a potential explanation for the observed modulation of disease progression in HSP70 mutants. Notably, the results also point to possible interactions with key enzymes in host physiology, including catalase 2, essential for ROS metabolism, and nitrilase, critical for auxin biosynthesis and root gall formation. These interactions highlight the potential involvement of CEO96729 in manipulating host cellular processes and raise the intriguing possibility of an unexpected role for this pathogen-derived HSP70 ortholog within the host cell. Collectively, our study highlights the multifaceted roles of HSP70 proteins in Plasmodiophora pathogenicity and host-pathogen interactions, offering insights into chaperone-mediated processes in plant immunity and infection dynamics.