A mechanistic understanding of community ecology requires tackling the nonadditive effects of multispecies interactions, a challenge that necessitates integration of ecological and molecular complexity-- namely moving beyond pairwise ecological interaction studies and the ‘gene at a time’ approach to mechanism. Here, we investigate the consequences of multispecies mutualisms for the structure and function of genome-wide coexpression networks for the first time, using the tractable and ecologically-important interaction between legume Medicago truncatula, rhizobia, and mycorrhizal fungi. First, we found that genes whose expression is affected nonadditively by multiple mutualists are more highly connected in gene networks than expected by chance and had 94% greater network centrality than genes showing additive effects, suggesting that nonadditive genes may be key players in the widespread transcriptomic responses to multispecies symbioses. Second, multispecies mutualisms substantially changed coexpression network structure of host plants and symbionts. Less than 50% of the plant and 10% of mycorrhizal fungi coexpression modules detected with rhizobia present were preserved in its absence, indicating that third-party mutualists can cause significant rewiring of plant and fungal molecular networks. Third, we identified unique sets of coexpressed genes that explain variation in plant performance only when multiple mutualists were present. Finally, an ‘across-symbiosis’ approach identified sets of coexpressed plant and mycorrhizal genes that were significantly associated with plant performance, were unique to the multiple mutualist context, and suggested coupled responses across the plant-mycorrhizal interaction to third-party mutualists. Taken together, these results show multispecies mutualism have substantial effects on the molecular interactions in host plants, microbes, and across symbiotic boundaries.