Summary Understanding how soil microbial communities influence plant interactions with other organisms, and how this varies with characteristics of the interacting organisms, is important for multiple systems. Solanum spp. are a suitable model for trophic interactions in studies of agricultural and natural systems and can also provide useful corollaries in invaded systems. This study examined the influence of soil mutualist arbuscular mycorrhizal (AM) fungi on growth of different Solanum types fed on by the potato aphid, Macrosiphum euphorbiae, in relation to the presence of the aphid facultative endosymbiont Hamiltonella defensa. Four Solanum types comprising two wild species, S. berthaultii and S. polyadenum, and two accessions of S. tuberosum, were grown with or without AM fungi and infested with one of four clonal lines of a single M. euphorbiae genotype (two with and two without H. defensa). Two experiments were conducted to (i) characterize plant responses to AM fungi and aphids and (ii) assess whether soil AM fungi could influence the success of the parasitoid wasp Aphidius ervi when attacking aphids reared on each Solanum type. In both experiments, similar patterns of plant biomass were observed in relation to AM fungal and aphid treatments. Solanum biomass depended on plant type and aphid infection with H. defensa. Plants exposed to aphids harbouring H. defensa had smaller root biomass, and therefore total plant biomass, compared to plants infested with H. defensa‐free aphids. M. euphorbiae performance varied with aphid clonal line, Solanum type and the presence of AM fungi. Parasitoid success, measured as the proportion of aphids from which a wasp emerged, was highest from aphids that had fed on plants colonized by AM fungi, although this result also varied with Solanum type and aphid clonal line. Synthesis. The presence of soil AM fungi, combined with within‐species plant and insect variation in key traits, can have subtle – but significant – effects on plant fitness and insect success. This study highlights the importance of exploring genotypic variation in plant and pest responses to soil microbiota to identify suitable biocontrol options.