Members of Clavibacter spp. are economically important bacterial plant pathogens infecting a set of diverse agricultural crops (e.g. alfalfa, corn, potato, tomato, and wheat). Tomato-associated Clavibacter spp. strains occupy a great portion of genetic diversity of the genus, and C. michiganensis sensu stricto (formerly C.michiganensis subsp. michiganensis) causing bacterial canker disease considered one of the destructive seed-borne agents of the crop worldwide. However, current taxonomic descriptions of the genus do not reflect the existing diversity of the strains, resulting in unsatisfactory consequences in quarantine surveys for the pathogens. In this study, we used all the available genome sequences of Clavibacter spp. strains − including the type strains of newly described subspecies − to provide a precise insight into the diversity of tomato-associated members of the genus, and further clarify taxonomic status of the strains using genotypic and phenotypic features. Results of phylogenetic analyses revealed the existence of nine hypothetical new species among the investigated strains. None of the three new subspecies (i.e. C. michiganensis subsp. californiensis, C. michiganensis subsp. chilensis and C. michiganensis subsp. phaseoli) is included within the tomato-pathogenic C. michiganensis sensu stricto lineage. Although comparative genomics revealed the lack of chp and tomA pathogenicity determinant gene clusters in the non-pathogenic strains, a number of pathogenicity related genes were noted to be present in all the strains regardless of their pathogenicity characteristics. Altogether, our results advocate a need for a formal taxonomic reconsideration of tomato-associated Clavibacter spp. strains to facilitate differentiation of the lineages in quarantine inspections.