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<i>Ustilaginoidea virens</i> is an ascomycetous fungus that causes rice false smut, an emerging disease around the world. The disease causes significant grain yield and quality loss in rice. Despite economic impact of the disease, little is known about the pathogenicity of <i>U. virens</i>. Through genome analyses, we revealed that the pathogen has a less extensive polysaccharide degradation machinery, particularly no pectin lyases, and thus minimizes the induction of host immunity by restricting the release of cell wall fragments, which is a typical feature for biotrophic pathogens. In addition, the pathogen possesses reduced gene inventories for nutrient uptake and secondary metabolism, which may result from adaptations to the specific floret infection. Evolutionarily,<i> U. virens </i>is close to the entomopathogenic <i>Metarhizium </i>spp., suggesting potential host jumping across kingdoms. Transcriptome analyses indicate that a specific set of genes for secreted proteins and secondary metabolism play important roles in virulence and pathogenicity of <i>U. virens</i>. Furthermore, eight candidate effectors were experimentally demonstrated to induce hypersensitive responses in <i>Nicotiana benthamiana</i>. And 18 effectors were found to suppress plant innate immunity in <i>N. benthamiana</i> and in rice. Together, these results offer new insights into molecular mechanisms of evolution, biotrophy and pathogenesis of <i>U. virens</i>. Some strategies for disease management are also discussed.