Summary Little is known about how sex differences in root zone characteristics, such as contents of allelochemicals and soil microbial composition, mediate intra‐ and intersexual interactions in dioecious plants. We examined the processes and mechanisms of sex‐specific belowground interactions mediated by allelochemicals and soil microorganisms in Populus cathayana females and males in replicated 30‐yr‐old experimental stands in situ and in a series of controlled experiments. Female roots released a greater amount and more diverse phenolic allelochemicals into the soil environment, resulting in growth inhibition of the same sex neighbors and deterioration of the community of soil microorganisms. When grown with males, the growth of females was consistently enhanced, especially the root growth. Compared with female monocultures, the presence of males reduced the total phenolic accumulation in the soil, resulting in a shift from allelopathic inhibition to chemical facilitation. This association was enhanced by a favorable soil bacterial community and increased bacterial diversity, and it induced changes in the orientation of female roots. Our study highlighted a novel mechanism that enhances female performance by males through alterations in the allelochemical content and soil microbial composition. The possibility to improve productivity by chemical mediation provides novel opportunities for managing plantations of dioecious plants.