The ancient African crop, finger millet, has broad resistance to pathogens including the toxigenic fungus Fusarium graminearum. Here we report the discovery of a novel plant defence mechanism, resulting from an unusual symbiosis between finger millet and a root-inhabiting bacterial endophyte, M6 (Enterobacter sp.). Seed-coated M6 swarms towards Fusarium attempting to penetrate root epidermis, induces growth of root hairs which then bend parallel to the root axis, then forms biofilm-mediated microcolonies, resulting in a remarkable, multi-layer root hair-endophyte stack (RHESt). RHESt results in a physical barrier that prevents entry and/or traps F. graminearum which is then killed. Thus M6 creates its own specialized killing microhabitat. M6 killing requires c-di-GMP-dependent signalling, diverse fungicides and xenobiotic resistance. Further molecular evidence suggests long-term host-endophyte-pathogen co-evolution. The end-result of this remarkable symbiosis is reduced DON mycotoxin, potentially benefiting millions of subsistence farmers and livestock. RHESt demonstrates the value of exploring ancient, orphan crop microbiomes.