Tilletia indica (Ti) - a quarantined fungal pathogen of wheat and its pathogenesis is chiefly governed by pathogen effectors secreted inside the host plant. The de novo genome sequencing of several field isolates and stages available could be used for understanding the molecular pathogenesis. The presence of gaps and low coverage of assembled genomes poses a problem in accurate functional annotation of such functions. In the present study attempts were made to improve the Ti draft genome through reconciliation of globally available datasets of three highly virulent monoteliospore cultures of Ti field isolates. It has sequence depth of 107x and N50 scaffold size of 80,772 (more than 26 times as large as achieved in the draft assembly) with highest sequence contiguity, more accurate and nearly complete. Functional annotation revealed that Ti genome contains 9209 genes evolved with many expanded gene families and arranged mostly in a cluster. About 79% of Ti genes were orthologous to other basidiomycetes fungi, Around 7.93% proteins were having secretary signals and 6.66% were identified as highly virulent pathogenicity genes. Using improved Ti genome as a reference, the genomic variation was assessed with respect to repeats, SNPs/InDel, gene families and correct set of virulence associated genes during its life cycle. The comparative intra-species, inter-stage and inter-species genomic variation will have broader implications to understand the gene regulatory networks involved in growth, mating and virulence behaviour of Tilletia f. spp. and also for better appreciation of fungal biology and disease management.