Apple valsa canker (AVC), caused by Valsa mali, inflicts substantial annual economic losses in apple production. Transmembrane proteins in plant pathogenic fungi mediate fungus–host interactions and regulate fungal growth and pathogenicity. However, their molecular mechanisms in the V. mali–apple pathosystem remain elusive. In this study, we demonstrated that transmembrane protein VmEM1 exhibits significantly upregulated expression during the early stage of V. mali infection in apple. The virulence of the VmEM1 deletion mutant (ΔVmEM1) was markedly attenuated, indicating that VmEM1 is essential for the full pathogenicity of V. mali. Notably, VmEM1 exerts dual roles: overexpression of VmEM1 attenuates V. mali pathogenicity while activating host immune responses. Purified VmEM1^ECD induced the accumulation of reactive oxygen species (ROS) and callose in Nicotiana benthamiana, enhanced N. benthamiana resistance to pathogens, and triggered cell death in a BAK1-, SOBIR1-, HSP90-, and SGT1-associated manner. Additionally, purified VmEM1^ECD promoted ROS and callose accumulation, as well as the expression of immune-related marker genes in apple tissues, thereby enhancing apple resistance to V. mali. Collectively, our findings reveal that VmEM1 acts as both a key virulence factor and an immune elicitor, providing novel insights into the pathogenic mechanism of V. mali and the molecular basis of the V. mali–apple interaction.