Microbes and plants exist within complex networks of interacting plant and microbial species. Our work explores the roles of plant community diversity, plant host, and fungal and bacterial species interactions in determining the pathogen-suppressive potential and composition of soil microbiomes, and the consequences for plant productivity. Unraveling the complex interactions among plants and soil microbiomes can suggest novel insights for active management of soil microbes to support plant productivity. Our results show that rhizosphere Streptomyces associated with the same plant host are significantly more pathogen-suppressive when the host grew in monoculture vs. within a high-diversity plant community. In contrast, populations of Streptomyces in the rhizosphere of plant hosts growing in high-diversity communities are more niche-differentiated than populations associated with the same host in monoculture. These data suggest that plant community diversity plays a critical role in determining the likelihood of antagonistic arms race coevolution vs. niche differentiation among sympatric soil populations, with significant implications for plant disease suppression. Fusarium populations also show evidence of coevolutionary interactions with Streptomyces. Fusarium are significantly better at inhibiting sympatric than allopatric populations of Streptomyces, and inhibition is positively correlated with niche overlap between sympatric, but not allopatric, Fusarium and Streptomyces. This work illustrates how diffuse networks of species interactions over diverse spatial scales contribute to determining the antagonistic potential of indigenous soil microbes, and suggests specific management approaches targeting species interactions that may offer potential for sustainable disease control.