Listeria monocytogenes is a foodborne pathogen that can cause invasive disease with high mortality in immunocompromised individuals and can survive and persist in a variety of environments for a long time. This study aims to investigate the genomic factors that contribute to the persistence of L. monocytogenes in food-associated environments by comparing the genomic features of persistent and non-persistent contamination strains in food retail markets in Zigong, China. Sixty-eight strains of L. monocytogenes were isolated from one retail market (M1 market) while the other 15 strains were from another seven markets (M2-M8 markets) in the same city. Whole-genome multilocus sequence typing (wg-MLST) and the whole-genome single nucleotide polymorphism (wg-SNP) analysis were performed. Three persistent contamination routes were identified in the M1 market, caused by 2 clusters (A and B) and a wgST31 type. Cluster A isolates were associated with the persistent contamination in a raw meat stall (M1-S77) while Cluster B isolates caused persistent contamination in aquatic foods stalls. Five wgST31 isolates caused persistent contamination in a single aquatic stall (M1-S65). A pLM1686-like plasmid was found in all Cluster A isolates. A novel plasmid pLM1692, a truncated pLM1686 plasmid losing the cadmium and other heavy metal resistance genes were conserved in all wgST31 persistent isolates. By comparing persistent and putative non-persistent isolates, four genes that were all located in the prophage comK might be associated with persistence. These findings enhanced our understanding of the underlying mechanisms of contamination and assist in formulating targeted strategies for the prevention and control of L. monocytogenes transmission from the food processing chain to humans.