Pratylenchus coffeae is a widespread migratory endoparasitic nematode that causes substantial yield losses across a broad range of crops. Successful parasitism depended on the secretion of effector proteins that modulate host cellular processes. In this study, we identified a novel β-1,4-endoglucanase effector, PcENG3, which was specifically expressed in the esophageal gland cell and gonadal tissues of P. coffeae and was significantly upregulated during parasitic stages. A yeast signal sequence trap assay confirmed the N-terminal signal peptide of PcENG3 was functional, suggesting its potential for secretion. Silencing PcENG3 in P. coffeae markedly impaired its infectivity on maize (Zea mays L.). Transgenic expression of PcENG3 in Arabidopsis thaliana suppressed flg22-triggered reactive oxygen species (ROS) accumulation, leading to enhanced susceptibility to nematode infection. Yeast two-hybrid and luciferase complementation imaging assays revealed a direct interaction between PcENG3 and maize ZmTCTP2a, a translationally controlled tumor protein involved in cell proliferation and immune regulation. Notably, suppression of ZmTCTP2a expression in maize increased susceptibility to P. coffeae and compromised basal immunity against multiple pathogens. Collectively, our findings uncovered a previously uncharacterized effector-host interaction in which PcENG3 targeted ZmTCTP2a to suppress immunity and alter root cap cell proliferation and differentiation, thereby promoting nematode parasitism. This work provided new insights into the molecular mechanisms underlying P. coffeae pathogenicity and host susceptibility.