Root-feeding herbivores can affect plant performance and the composition of natural plant communities, but there is little information about the mechanisms that control root herbivores in natural systems. This study explores the interactions between the pioneer dune grass Ammophila arenaria, arbuscular mycorrhizal fungi (AMF) and the root-feeding nematode Pratylenchus penetrans. Our objectives were to determine whether AMF can suppress nematode infection and reproduction and to explore the mechanisms of nematode control by AMF. A sequential inoculation experiment and a split-root experiment were designed to analyse the importance of plant tolerance and resistance and of direct competition between AMF and P. penetrans for the root herbivore and the plant. Root infection and multiplication of P. penetrans were significantly reduced by the native inoculum of AMF. Plant preinoculation with AMF further decreased nematode colonization and reproduction. Nematode suppression by AMF did not occur through a systemic plant response but through local mechanisms. Our results suggest that AMF are crucial for the control of root-feeding nematodes in natural systems and illustrate that locally operating mechanisms are involved in this process.