False smut disease of rice caused by Ustilaginoidea virens, is an emerging threat to rice cultivation worldwide due to its detrimental effects on grain yield and quality. False smut disease severity was 4.44‒17.22% during a roving survey in Kharif 2016 in the four different rice ecosystems of Karnataka, India. Further, 15 pathogen isolates representing four different ecosystems were studied for their virulence and morphometric diversity. Among the 15 strains studied, most virulent strains Uv-Gvt was selected for whole genome sequencing in Illumina NextSeq 500 platform using 2 × 150 bp sequencing chemistry. The total assembled genome of Uv-Gvt was 26.96 Mb, which comprised of 9157 scaffolds with an N50 value of 15,934 bp and 6628 protein-coding genes. Next, the comparative genomic study revealed a similar gene inventory as UV-8b and MAFF 236576 strains reported from China and Japan, respectively. But, 1756 genes were unique to Uv-Gvt strain. The Uv-Gvt genome harbors 422 putative host–pathogen interacting genes compared to 359 and 520 genes in UV-8b and MAFF 236576 strains, respectively. The variant analysis revealed low genetic diversity (0.073‒0.088%) among U. virens strains. Further, phylogenetic analysis using 250 single copy orthologs genes of U. virens revealed a distinct phylogeny and an approximate divergence time. Our study, report the genomic resource of rice false smut pathogen from India, where the disease originated, and this information will have broader applicability in understanding the pathogen population diversity.