The present study was designed to evaluate the potential presence and features of Listeria monocytogenes in different commercial and native poultry breeds. Overall, the isolation of L. monocytogenes strains from different chicken species was 42/550 (7.6%). L. monocytogenes showed high resistance to streptomycin (83.3%) and amoxicillin/clavulanic acid (78.5%) and was highly sensitive to vancomycin, gentamycin, and chloramphenicol. Multiple drug resistance (MAR) index values for 59.5% of the isolates were greater than 0.2. L. monocytogenes strains were screened for five virulence factors associated with genes, namely inlA, actA, hlyA, iap, and inlB. The presence of the five virulence genes were 83.3%, 66.6%, 59.5%, 57.1%, and 45.2% for actA, iap, inlA, hlyA, and inlB, respectively, in the identified L. monocytogenes isolates. Moreover, histopathological examination revealed marked changes in the brain and heart as the most affected tissues. Both the cerebral hemispheres and cerebellum were affected and exhibited marked encephalitis represented by diffuse congestion of cerebral blood vessels. These findings suggest that poultry products may play a role in the zoonotic spread and transmission of multidrug-resistant and virulent L. monocytogenes, which can pose a health risk at human-poultry interface, especially in the absence of stringent hygienic standards and preventive measures.