Following the recent listeriosis outbreak in South Africa, this study was carried out to assess the safety level of various common ready-to-eat foods (RTE) obtained from supermarkets and grocery stores in major towns and cities within the Amathole, Chris Hani and Sarah Baartman Districts Municipalities, Eastern Cape Province, South Africa. A sum of 239 food samples was collected from these locations, and Listeria monocytogenes (Lm) was isolated in line with the recommended techniques by the International Organization for Standardization EN ISO 11290:2017 parts 1 and 2. Identification of the pathogen and detection of various associated virulence genes was done using Polymerase Chain Reaction (PCR) techniques. From the RTE food samples processed, Lm was detected in 107 (44.77%) of the samples. Russian sausage was the most contaminated (78.57%), followed by sliced polony (61.90%), muffins (58.33%), polony (52.63%), and pies (52.38%), while all vetkoek samples examined were negative for Lm. Although the prevalence of Lm in the food samples was very high, concentrations were generally < 100 CFU/g. Strains of Lm recovered from the RTE foods were predominantly epidemiological strains belonging to serotypes 1/2a, 1/2b and 4b. The prevalence of 10 virulence genes including the inlA, InlC, inlJ, plcA, hlyA, plcB, prfA, mpl, inlB, and actA were detected among Lm isolates. Most of the isolates (69.07%) demonstrated the potential for biofilm formation and were categorized as weak (14.95%), moderate (13.40%) and strong (40.72) biofilm formers. Furthermore, molecular typing revealed high levels of genetic diversity among Lm isolates. The findings of this investigation suggested that the presence of Lm in the RTE foods may constitute potential threats to the food sector and could pose public health hazards to consumers, particularly the high-risk group of the population. We, therefore, recommend that adequate food monitoring for safety and proper regulation enforcement in the food sector must be ensured to avoid any future listeriosis outbreak that could be linked to RTE foods in South Africa.