Tomato canker is a geographically widespread and lethal disease of tomato. This seed-borne disease is caused by Clavibacter michiganensis subsp. michiganensis (Cmm) which produces copious amounts of extracellular polysaccharide (EPS). The aim of this study was to better understand the genomic determinants involved in pathogenicity. We have sequenced three strains using PacBio: virulent & EPS-producing, virulent & non-EPS-producing, and non-virulent & EPS-producing. Comparative genomic analyses revealed no truncated clusters associated with EPS production; however, large-scale rearrangement events were observed. Plasmid organization was different for each strain and the plasmid sequences showed significant differences in their genomic constituents. Plasmids pCM1 and pCM2 were present in virulent EPS-producing and virulent non-EPS-producing strains, respectively, but showed high discrepancy when aligned with reference genome NCPPB 382. Non-pathogenic strains showed disrupted and/or truncated pathogenicity islands (tomA and chp clusters). Scanning electron microscopy and qPCR results confirmed that the EPS-producing virulent strain colonized the host more rapidly, whereas, non-virulent strain showed no colonization of the stem vascular tissue (lacked the colonization facilitator gene: chpG), although it was detected in the root samples.