The similarity of theListeria innocuagenome withListeria monocytogenesand their presence in the same niche may facilitate gene transfer between them. A better understanding of the mechanisms responsible for bacterial virulence requires an in-depth knowledge of the genetic characteristics of these bacteria. In this context, draft whole genome sequences were completed on fiveL. innocuaisolated from milk and dairy products in Egypt. The assembled sequences were screened for antimicrobial resistance and virulence genes, plasmid replicons and multilocus sequence types (MLST); phylogenetic analysis of the sequenced isolates was also performed. The sequencing results revealed the presence of only one antimicrobial resistance gene,fosX, in theL. innocuaisolates. However, the five isolates carried 13 virulence genes involved in adhesion, invasion, surface protein anchoring, peptidoglycan degradation, intracellular survival, and heat stress; all five lacked theListeriaPathogenicity Island 1 (LIPI-1) genes. MLST assigned these five isolates into the same sequence type (ST), ST-1085; however, single nucleotide polymorphism (SNP)-based phylogenetic analysis revealed 422–1,091 SNP differences between our isolates and global lineages ofL. innocua. The five isolates possessed an ATP-dependent protease (clpL) gene, which mediates heat resistance, on arep25 type plasmids. Blast analysis ofclpL-carrying plasmid contigs showed approximately 99% sequence similarity to the corresponding parts of plasmids ofL. monocytogenesstrains 2015TE24968 and N1-011A previously isolated from Italy and the United States, respectively. Although this plasmid has been linked toL. monocytogenesthat was responsible for a serious outbreak, this is the first report ofL. innocuacontainingclpL-carrying plasmids. Various genetic mechanisms of virulence transfer amongListeriaspecies and other genera could raise the possibility of the evolution of virulent strains ofL. innocua. Such strains could challenge processing and preservation protocols and pose health risks from dairy products. Ongoing genomic research is necessary to identify these alarming genetic changes and develop preventive and control measures.