Subspecies of Clavibacter michiganensis are important phytobacterial pathogens causing devastating diseases in several agricultural crops. The genome organizations of these pathogens are poorly understood. Here, the complete genomes of 5 subspecies (C. michiganensis subsp. michiganensis, Cmi; C. michiganensis subsp. sepedonicus, Cms; C. michiganensis subsp. nebraskensis, Cmn; C. michiganensis subsp. insidiosus, Cmi and C. michiganensis subsp. capsici, Cmc) were analyzed. This study assessed the taxonomic position of the subspecies based on 16S rRNA and genome-based DNA homology and concludes that there is ample evidence to elevate some of the subspecies to species-level. Comparative genomics analysis indicated distinct genomic features evident on the DNA structural atlases and annotation features. Based on orthologous gene analysis, about 2300 CDSs are shared across all the subspecies; and Cms showed the highest number of subspecies-specific CDS, most of which are mobile elements suggesting that Cms could be more prone to translocation of foreign genes. Cms and Cmi had the highest number of pseudogenes, an indication of potential degenerating genomes. The stress response factors that may be involved in cold/heat shock, detoxification, oxidative stress, osmoregulation, and carbon utilization are outlined. For example, the wco-cluster encoding for extracellular polysaccharide II is highly conserved while the sucrose-6-phosphate hydrolase that catalyzes the hydrolysis of sucrose-6-phosphate yielding glucose-6-phosphate and fructose is highly divergent. A unique second form of the enzyme is only present in Cmn NCPPB 2581. Also, twenty-eight plasmid-borne CDSs in the other subspecies were found to have homologues in the chromosomal genome of Cmn which is known not to carry plasmids. These CDSs include pathogenesis-related factors such as Endocellulases E1 and Beta-glucosidase. The results presented here provide an insight of the functional organization of the genomes of five core C. michiganensis subspecies, enabling a better understanding of these phytobacteria.