Root rot disease has seriously restricted the development of the apple industry Worldwide. After being infected by pathogens, the microbial communities of rhizosphere soil and leaves may change. We found that apple and persimmon intercropping can reduce the occurrence of apple root rot achieving a relative control efficacy of 80.3% following persimmon intercropping. Here, we investigate the effect of intercropping with persimmon tree on rhizosphere microbiome and leaf endophytes. For this, we tested the rhizosphere soil and leaves of healthy and infected apple trees during intercropping. The soil and leaves of healthy and infected root rot apple trees, persimmon trees, and intercropping were collected (during sampling time, apple trees were 5 years old, and persimmon trees were 3 years old). The high-throughput sequencing was performed on the Illumina Miseq platform to analyze the leaf endophytic bacterial and soil microbial communities. We further revealed that infection by root rot pathogens severely impacts the synergistic effects between endophytes and the composition of rhizosphere microbial communities. The intercropping between apple and persimmon trees can modulate apple leaf endophytes and rhizosphere microbial communities. Importantly, the relative abundance of Pantoea and Serratia increased significantly in the leaves of apple trees affected by root rot. We argue that bacteria such as Pantoea and Serratia are conducive to the occurrence of root rot. Notably, Bacillus and Trichoderma were significantly reduced in the rhizosphere of apples with root rot trees; however, persimmon trees and apple trees can maintain the relative abundance of beneficial species or improve the abundance compared with healthy apple trees. The overall study concludes that intercropping apples and persimmons maintains the beneficial microbial balance and plant growth and helps to prevent dysbiosis caused by pathogens. Based on this shift in microbiome balance, a management strategy for apple root rot is discussed.