Abstract Plants typically interact with multiple above‐ and below‐ground organisms simultaneously, with their symbiotic relationships spanning a continuum ranging from mutualism, such as with arbuscular mycorrhizal fungi (AMF), to parasitism, including symbioses with plant‐parasitic nematodes (PPN). Although research is revealing the patterns of plant resource allocation to mutualistic AMF partners under different host and environmental constraints, the root ecosystem, with multiple competing symbionts, is often ignored. Such competition is likely to heavily influence resource allocation to symbionts. Here, we outline and discuss the competition between AMF and PPN for the finite supply of host plant resources, highlighting the need for a more holistic understanding of the influence of below‐ground interactions on plant resource allocation. Based on recent developments in our understanding of other symbiotic systems such as legume–rhizobia and AMF‐aphid‐plant, we propose hypotheses for the distribution of plant resources between contrasting below‐ground symbionts and how such competition may affect the host. We identify relevant knowledge gaps at the physiological and molecular scales which, if resolved, will improve our understanding of the true ecological significance and potential future exploitation of AMF‐PPN‐plant interactions in order to optimize plant growth. To resolve these outstanding knowledge gaps, we propose the application of well‐established methods in isotope tracing and nutrient budgeting to monitor the movement of nutrients between symbionts. By combining these approaches with novel time of arrival experiments and experimental systems involving multiple plant hosts interlinked by common mycelial networks, it may be possible to reveal the impact of multiple, simultaneous colonizations by competing symbionts on carbon and nutrient flows across ecologically important scales.