Rhizoctonia solani is a fungal species complex that causes necrotrophic crop diseases. It comprises several anastomosis groups, some of which include intra-subgroups, such as AG-1 IA and AG-1 IB, exhibiting varying pathogenicity. Owing to its heterozygous and multinucleate features, genomic analyses of R. solani are still challenging, and understanding of its genetic diversity and genic components is limited. In this study, in order to elucidate the molecular basis of this phytopathogen complex, an integrated transcriptome analysis was undertaken for three subgroups of AG-1, i.e. AG-1 IA, AG-1 IB, and AG-1 IC. Sequence variations suggested substantial evolutionary distances within AG-1. Transcript simple sequence repeats showed comparable characteristics among AG-1, but contained polymorphic sites. Intra-subgroup polymorphisms suggested varying genic heterozygosity within AG-1, suggesting their independent evolutionary trajectory. Sequences of pathogenic factors, phytotoxin biosynthesis pathway enzymes, secreted lignocellulosic enzymes, secreted reactive oxygen species detoxification enzymes, apoplastic/cytoplasmic effector candidates, were conserved among those subgroups. dN/dS ratios of a secretome subset suggested core secreted proteins in AG-1 and distinct evolution of Cys-rich small secreted proteins after differentiation of AG-1 subgroups. Identification of likely pathogenic factors including allergen protein homologues, oxidative phosphorylation and ethylene biosynthesis pathways, and diversification of polysaccharide monooxygenases provides molecular insight into key genomic components that play a role in R. solani pathogenesis.