Aphis gossypii Glover is a prevalent phytophagous insect that inflicts significant damage on cucumber plants. Recent studies have provided insights into plant communication and signal transduction within conspecifics. However, understanding of the effect of these communication mechanisms on adjacent cucumbers and their resident aphids, especially in the context of an aphid infestation, is still in its early stages. Utilizing a partitioned root configuration, a tendency for aphids to gather on nearby cucumber leaves of non-infested plants was observed. Furthermore, neighboring plants near aphid-infested cucumber plants showed a reduction in aphid reproduction rates. Concurrently, these plants exhibited a significant increase in reactive oxygen species (ROS) levels, along with enhanced defensive and antioxidant enzymatic responses. Analysis of the microbial community in the rhizosphere showed significant differences in species composition among the samples. Among these, the bacterial families Microbacteriaceae and Rhizobiaceae, along with the fungal species Leucocoprinus ianthinus and Mortierella globalpina, exhibited increases in their relative abundance in cucumber seedlings located near aphid-infested plants. Significantly, this study unveiled robust correlations between dominant microbial phyla and physiological indicators, primarily associated with aphid resistance mechanisms in plants. The results show that aphid-infested cucumber plants trigger oxidative stress responses in adjacent seedlings through complex interplant communication mechanisms. In addition, these plants cause changes in the composition of the rhizospheric microbial community and the physiological activity of neighboring plants, consequently boosting their natural resistance to aphids. This study provides essential theoretical foundations to guide the development of sustainable strategies for managing cucumber aphids. © 2024 Society of Chemical Industry.