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The <i>Thinopyrum elongatum Fhb7E</i> locus has been proven to confer outstanding resistance to Fusarium Head Blight (FHB) when transferred into wheat, minimizing yield loss and mycotoxin accumulation in grains. Despite their biological relevance and breeding implications, the molecular mechanisms underlying the resistant phenotype associated with <i>Fhb7E</i> have not been fully uncovered. To gain a broader understanding of processes involved in this complex plant–pathogen interaction, we analysed via untargeted metabolomics durum wheat (DW) rachises and grains upon spike inoculation with <i>Fusarium graminearum</i> (<i>Fg</i>) and water. The employment of DW near-isogenic recombinant lines carrying or lacking the <i>Th. elongatum</i> chromosome 7E region including <i>Fhb7E</i> on their 7AL arm, allowed clear-cut distinction between differentially accumulated disease-related metabolites. Besides confirming the rachis as key site of the main metabolic shift in plant response to FHB, and the upregulation of defence pathways (aromatic amino acid, phenylpropanoid, terpenoid) leading to antioxidants and lignin accumulation, novel insights were revealed. <i>Fhb7E</i> conferred constitutive and early-induced defence response, in which specific importance of polyamine biosynthesis, glutathione and vitamin B₆ metabolisms, along with presence of multiple routes for deoxynivalenol detoxification, was highlighted. The results suggested <i>Fhb7E</i> to correspond to a compound locus, triggering a multi-faceted plant response to <i>Fg</i>, effectively limiting <i>Fg</i> growth and mycotoxin production.