Listeria monocytogenes is a foodborne pathogen of significant concern for the food industry due to its remarkable ability to persist through safety control efforts, posing a subsequent health threat to consumers. Understanding the microbial communities coexisting with L. monocytogenes in food processing environments provides insights into its persistence mechanisms. We investigated the microbial communities on non-food contact surfaces in a facility producing ready-to-eat foods, known to harbour a ST121 L. monocytogenes strain over multiple years. A 10-week sampling period was coordinated with the company and public health authorities. Metagenomic analysis revealed a stable microbial composition dominated by Pseudomonas fluorescens. While highly related populations were present in high-care production zones, distinctive taxa characteristic of specific areas were observed (e.g., Sphingomonas aerolata). Although Listeria spp. were not detected in metagenomes, they were detected in cultured samples, suggesting low relative abundance in factory settings. The findings suggest that a stable resident microbiota, with distinct adaptations to different areas within the factory, was selected for by their collective ability to survive control efforts in this environment. Listeria spp. was a member of this microbial community, albeit at low abundance, and may likewise benefit from the mutualism of the overall microbial community.