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The genus <i>Listeria</i> now comprises up to now 21 recognized species and six subspecies, with <i>L. monocytogenes</i> and <i>L. innocua</i> as the most prevalent sensu stricto associated species. Reports focusing on the challenges in <i>Listeria</i> detection and confirmation are available, especially from food-associated environmental samples. <i>L. innocua</i> is more prevalent in the food processing environment (FPE) than <i>L. monocytogenes</i> and has been shown to have a growth advantage in selective enrichment and agar media. Until now, the adaptive nature of <i>L. innocua</i> in FPEs has not been fully elucidated and potential persistence in the FPE has not been observed. Therefore, the aim of this study is to characterize <i>L. innocua</i> (<i>n</i> = 139) and <i>L. monocytogenes</i> (<i>n</i> = 81) isolated from FPEs and cheese products collected at five dairy processing facilities (A&#8722;E) at geno- and phenotypic levels. Biochemical profiling was conducted for all <i>L. monocytogenes</i> and the majority of <i>L. innocua</i> (<i>n</i> = 124) isolates and included a rhamnose positive reaction. <i>L. monocytogenes</i> isolates were most frequently confirmed as PCR-serogroups 1/2a, 3a (95%). Pulsed-field gel electrophoresis (PFGE)-typing, applying the restriction enzymes <i>AscI</i>, revealed 33 distinct <i>Listeria</i> PFGE profiles with a Simpson&#8217;s Index of Diversity of 0.75. Multi-locus sequence typing (MLST) resulted in 27 STs with seven new <i>L. innocua</i> local STs (ST1595 to ST1601). <i>L. innocua</i> ST1597 and ST603 and <i>L. monocytogenes</i> ST121 and ST14 were the most abundant genotypes in dairy processing facilities A&#8722;E over time. Either SSI-1 (ST14) or SSI-2 (ST121, all <i>L. innocua</i>) were present in successfully FPE-adapted strains. We identified housekeeping genes common in <i>Listeria</i> isolates and <i>L. monocytogenes</i> genetic lineage III. Wherever there are long-term contamination events of <i>L. monocytogenes</i> and other <i>Listeria</i> species, subtyping methods are helpful tools to identify niches of high risk.