Summary Meloidogyne enterolobii is an emerging root‐knot nematode species that overcomes most of the nematode resistance genes in crops. Nematode effector proteins secreted in planta are key elements in the molecular dialogue of parasitism. Here, we show the MeMSP1 effector is secreted into giant cells and promotes M. enterolobii parasitism. Using co‐immunoprecipitation and bimolecular fluorescent complementation assays, we identified glutathione‐S‐transferase phi GSTFs as host targets of the MeMSP1 effector. This protein family plays important roles in plant responses to abiotic and biotic stresses. We demonstrate that MeMSP1 interacts with all Arabidopsis GSTF. Moreover, we confirmed that the N‐terminal region of AtGSTF9 is critical for its interaction, and atgstf9 mutant lines are more susceptible to root‐knot nematode infection. Combined transcriptome and metabolome analyses showed that MeMSP1 affects the metabolic pathways of Arabidopsis thaliana, resulting in the accumulation of amino acids, nucleic acids, and their metabolites, and organic acids and the downregulation of flavonoids. Our study has shed light on a novel effector mechanism that targets plant metabolism, reducing the production of plant defence‐related compounds while favouring the accumulation of metabolites beneficial to the nematode, and thereby promoting parasitism.