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Background   Listeria monocytogenes  is a widespread foodborne pathogen that can cause listeriosis, a potentially fatal infection.  L. monocytogenes  is subdivided into four phylogenetic lineages, with the highest incidence of listeriosis occurring within lineage I followed by lineage II. Strains of  L. monocytogenes  differ in their phenotypic characteristics, including virulence. However, the genetic bases for these observed differences are not well understood, and current efforts to monitor  L. monocytogenes  in food consider all strains to be equally virulent. We use a comparative genomics approach to identify genes and single nucleotide polymorphisms (SNPs) in 174 clinical and food isolates of  L. monocytogenes  that potentially contribute to virulence or the capacity to adapt to food environments.    Results  No SNPs are significantly associated with food or clinical isolates. No genes are significantly associated with food or clinical isolates from lineage I, but eight genes consisting of multiple homologues are associated with lineage II food isolates. These include three genes which encode hypothetical proteins, the cadmium resistance genes  cadA  and  cadC , the multi-drug resistance gene  ebrB , a quaternary ammonium compound resistance gene  qac , and a regulatory gene. All eight genes are plasmid-borne, and most closed  L. monocytogenes  plasmids carry at least five of the genes (24/27). In addition, plasmids are more frequently associated with lineage II food isolates than with lineage II clinical isolates.    Conclusions  We identify eight genes that are significantly associated with food isolates in lineage II. Interestingly, the eight genes are virtually absent in lineage II outbreak isolates, are composed of homologues which show a nonrandom distribution among lineage I serotypes, and the sequences are highly conserved across 27 closed  Listeria  plasmids. The functions of these genes should be explored further and will contribute to our understanding of how  L. monocytogenes  adapts to the host and food environments. Moreover, these genes may also be useful as markers for risk assessment models of either pathogenicity or the ability to proliferate in food and the food processing environment.    Electronic supplementary material  The online version of this article (10.1186/s12864-018-5074-2) contains supplementary material, which is available to authorized users.

Genes significantly associated with lineage II food isolates of Listeria monocytogenes