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<i>Pinus</i> is an important economic tree species, but pine wilt disease (PWD) seriously threatens the survival of pine trees. PWD caused by <i>Bursaphelenchus xylophilus</i> is a major quarantine disease worldwide that causes significant economic losses. However, more information about its molecular pathogenesis is needed, resulting in a lack of effective prevention and treatment measures. In recent years, effectors have become a hot topic in exploring the molecular pathogenic mechanism of pathogens. Here, we identified a specific effector, BxNMP1, from <i>B. xylophilus</i>. In situ hybridization experiments revealed that <i>BxNMP1</i> was specifically expressed in dorsal gland cells and intestinal cells, and RT–qPCR experiments revealed that <i>BxNMP1</i> was upregulated in the early stage of infection. The sequence of <i>BxNMP1</i> was different in the avirulent strain, and when <i>BxNMP1</i>-silenced <i>B. xylophilus</i> was inoculated into <i>P. thunbergii</i> seedlings, the disease severity significantly decreased. We demonstrated that BxNMP1 interacted with the thaumatin-like protein PtTLP-L2 in <i>P. thunbergii</i>. Additionally, we found that the β-1,3-glucanase PtGLU interacted with PtTLP-L2. Therefore, we hypothesized that BxNMP1 might indirectly interact with PtGLU through PtTLP-L2 as an intermediate mediator. Both targets can respond to infection, and PtTLP-L2 can enhance the resistance of pine trees. Moreover, we detected increased salicylic acid contents in <i>P. thunbergii</i> seedlings inoculated with <i>B. xylophilus</i> when <i>BxNMP1</i> was silenced or when the PtTLP-L2 recombinant protein was added. In summary, we identified a key virulence effector of PWNs, BxNMP1. It positively regulates the pathogenicity of <i>B. xylophilus</i> and interacts directly with PtTLP-L2 and indirectly with PtGLU. It also inhibits the expression of two targets and the host salicylic acid pathway. This study provides theoretical guidance and a practical basis for controlling PWD and breeding for disease resistance.