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Summary Despite their ubiquitous nature, interactions between multiple micro‐organisms and their effects on host growth and each other's success have received limited scientific attention. In particular, grasses can be commonly infected by both endophytic fungi and viruses, which are typically transmitted by aphids. In this study, we investigated how an aphid‐transmitted viral pathogen and a symbiotic endophytic fungus altered host growth and allocation. We hypothesized that, by reducing aphid feeding, endophyte infection would lower viral titre and consequently decrease the negative effects of virus infection on host biomass production. In a greenhouse experiment, we manipulated fungal endophyte status and virus infection ( Barley Yellow Dwarf Virus – PAV ) of two tall fescue cultivars with different genetic backgrounds [KY 31 and pasture demonstration farm (PDF)]. In one cultivar (PDF), we also manipulated endophyte strain, using two strains that had been selected for differences in alkaloid production. We assessed host, virus and vector responses. As hypothesized, endophyte infection decreased reproduction and abundance of aphid vectors; however, in contrast to our hypothesis, this response by aphids did not impact viral titre. For both tall fescue cultivars, endophyte infection alleviated the negative effect of virus infection on the proportion of total plant biomass allocated to roots. On the other hand, for the KY 31 cultivar only, virus infection decreased tillering in endophyte‐infected individuals, but not endophyte‐free individuals. Within the PDF cultivar, both endophyte strains produced similar effects on host, virus and vector responses. Synthesis These results indicate that some of the beneficial effects provided by endophyte infection, particularly alleviating the negative effect of virus infection on the proportion of total plant biomass allocated to roots, do not arise strictly from altering host interactions with herbivores (aphids), but also occur by changing host responses to viral infection. Furthermore, these results emphasize the importance of exploring multispecies microbial interactions and genetic controls on these interactions in order to more fully understand their role in community‐ and ecosystem‐level dynamics.