Genus is a large assemblage of diverse microorganisms, not sharing a common evolutionary history. To clarify their evolutionary relationships and classification, we have conducted comprehensive phylogenomic and comparative analyses on 388 genomes. In phylogenomic trees, species formed 12 main clusters, apart from the "Aeruginosa clade" containing its type species, . In parallel, our detailed analyses on protein sequences from genomes have identified 98 novel conserved signature indels (CSIs), which are uniquely shared by the species from different observed clades/groups. Six CSIs, which are exclusively shared by species from the "Aeruginosa clade," provide reliable demarcation of this clade corresponding to the genus in molecular terms. The remaining 92 identified CSIs are specific for nine other species clades and the genera and which branch in between them. The identified CSIs provide strong independent evidence of the genetic cohesiveness of these species clades and offer reliable means for their demarcation/circumscription. Based on the robust phylogenetic and molecular evidence presented here supporting the distinctness of the observed species clades, we are proposing the transfer of species from the following clades into the indicated novel genera: Alcaligenes clade - gen. nov.; Fluvialis clade - gen. nov.; Linyingensis clade - gen. nov.; Oleovorans clade - gen. nov.; Resinovorans clade - gen. nov.; Straminea clade - gen. nov.; and Thermotolerans clade - gen. nov. In addition, descriptions of the genera , , , and are emended to include information for the CSIs specific for them. The results presented here should aid in the development of a more reliable classification scheme for species.