Guava wilt disease is caused by the fungus Nalanthamala psidii. The wilt disease results in large-scale destruction of orchards in South Africa, Taiwan, and several Southeast Asian countries. De novo assembly, annotation, and in-depth analysis of the N. psidii genome were carried out to facilitate the identification of characteristics associated with pathogenicity and pathogen evolution. The predicted secretome revealed a range of CAZymes, proteases, lipases and peroxidases associated with plant cell wall degradation, nutrient acquisition, and disease development. Further analysis of the N. psidii carbohydrate-active enzyme profile exposed the broad-spectrum necrotrophic lifestyle of the pathogen, which was corroborated by the identification of putative effectors and secondary metabolites with the potential to induce tissue necrosis and cell surface-dependent immune responses. Putative regulatory proteins including transcription factors and kinases were identified in addition to transporters potentially involved in the secretion of secondary metabolites. Transporters identified included important ABC and MFS transporters involved in the efflux of fungicides. Analysis of the repetitive landscape and the detection of mechanisms linked to reproduction such as het and mating genes rendered insights into the biological complexity and evolutionary potential of N. psidii as guava pathogen. Hence, the assembly and annotation of the N. psidii genome provided a valuable platform to explore the pathogenic potential and necrotrophic lifestyle of the guava wilt pathogen.