Staphylococcus aureus is a highly versatile pathogen in a large number of domestic animals, including avian species. To gain deeper insight into the epidemiology and diversity of S. aureus associated with articular disease in domestic turkeys, isolates were collected from infected foot joints of turkeys in Brittany (France). A total of 34 isolates were recovered and characterized by means of antimicrobial resistance, staphylococcal protein A typing, macrorestriction pulsed-field gel electrophoresis and micro-array analysis. Thirty isolates were identified as clonal complex (CC) 398 and methicillin-susceptible S. aureus (MSSA), one was identified as a methicillin-resistant S. aureus (MRSA) CC398 isolate, and the remaining were also MSSA and belonged to CC5, CC101, and CC121. Eleven different antimicrobial resistance patterns were detected, with most isolates resistant to penicillin and tetracycline. Based on all typing methods used, the 34 isolates could be divided into 22 different strains. Results on selected isolates, genotyped using microarrays, indicated a high homogeneity among pathogenic MSSA isolates from turkeys. Moreover, all isolates, except the unique MRSA isolate, carried specific φAvβ prophage avian-niche-specific genes, demonstrating the versatility of S. aureus to adapt to the specific ecological poultry niche.