Interactions between plants and microbiomes play a key role in ecosystem functioning, and are of broad interest due to their influence on nutrient cycling and plant protection. However, we do not yet have a complete understanding of how plant microbiomes are assembled. Here, for the first time, we show interactions between plant-associated microbial communities that drive their diversity and community composition. We manipulated soil microbial diversity, plant species, and herbivory, and found that soil microbial diversity influenced the herbivore-associated microbiome composition, but also plant species and herbivory influenced the soil microbiome composition. We used a novel approach, quantifying the relative strength of these effects, and demonstrated that the initial soil microbiome diversity explained the most variation in plant- and herbivore-associated microbial communities. Our findings strongly suggest that soil microbial community diversity is a driver of the composition of multiple associated microbiomes (plant and insect), and this has implications for the importance of management of soil microbiomes in multiple systems.