Abstract Both the phyllosphere and rhizosphere are inhabited by different kinds of microorganisms that are closely related to plant growth and health. However, it is not clear whether disease-resistant cultivars shape the microbiome to facilitate disease resistance. In this study, significant differences were found in the aboveground and belowground bacterial communities of disease-resistant and disease-susceptible cultivars grown in the same kiwifruit orchard. The phyllosphere of the resistant cultivar ‘Wanjin’ showed greater enrichment of Pseudomonas spp. and Sphingomonas spp. than the susceptible cultivar ‘Donghong’. The rhizosphere microbes of ‘Wanjin’ were less affected by field location, with significantly greater bacterial abundance than those of ‘Donghong’ and more bacteria with potential biocontrol properties. Pseudomonas syringae pv. actinidiae (Psa) infection significantly affected the microbiome of the phyllosphere of kiwifruit plants, especially that of ‘Donghong’. Resistant and susceptible kiwifruit cultivars exhibit distinct beneficial microbial recruitment strategies under Psa challenge. The phyllosphere of ‘Donghong’ in Jinzhai was enriched with Sphingomonas spp. and Pantoea spp. under Psa infection, while the rhizosphere of ‘Wanjin’ was enriched with Sphingomonas spp. and Novosphingobium spp. We further identified five key biomarkers within the microbial community associated with Psa infection. Inoculation experiments showed that Lysobacter sp. R34, Stenotrophomonas sp. R31, Pseudomonas sp. R10 and RS54, which were isolated from belowground compartments of ‘Wanjin’, could positively affect plant performance under Psa challenge. The combination use of Pseudomonas sp. R10 and Stenotrophomonas sp. R31 significantly improve the management of kiwifruit canker. Our findings provided novel insights into soil–microbe–plant interactions and the role of microbes in plant disease resistance and susceptibility.