Summary Plants simultaneously interact with a range of biotrophic symbionts, ranging from mutualists such as arbuscular mycorrhizal fungi (AMF), to parasites such as the potato cyst nematode (PCN). The exchange of mycorrhizal‐acquired nutrients for plant‐fixed carbon (C) is well studied; however, the impact of competing symbionts remains underexplored. In this study, we examined mycorrhizal nutrient and host resource allocation in potato with and without AMF and PCN using radioisotope tracing, whilst determining the consequences of such allocation. The presence of PCN disrupted C for nutrient exchange between plants and AMF, with plant C overwhelmingly obtained by the nematodes. Despite this, AMF maintained transfer of nutrients on PCN‐infected potato, ultimately losing out in their C for nutrient exchange with the host. Whilst PCN exploited the greater nutrient reserves to drive population growth on AMF–potato, the fungus imparted tolerance to allow the host to bear the parasitic burden. Our findings provide important insights into the belowground dynamics of plant–AMF symbioses, where simultaneous nutritional and nonnutritional benefits conferred by AMF to hosts and their parasites are seldom considered in plant community dynamics. Our findings suggest this may be a critical oversight, particularly in the consideration of C and nutrient flows in plant and soil communities.