Campylobacter is a leading cause of diarrhoea, and its presence in chickens is a significant risk for zoonotic infection. Poultry production is becoming increasingly intensive in Ethiopia and is incorporating more high-producing breeds into traditionally managed smallholdings, especially in peri-urban areas. This cross-sectional study sampled 219 household environments in one peri-urban and two rural areas of Ethiopia, and an additional 20 semi-intensive farms in the peri-urban district. Campylobacter was detected by polymerase chain reaction (PCR)-specific assays in 44 samples; 16 of which could be identified as C. jejuni. Flocks in the peri-urban area were at significantly greater odds of detection, including those which only kept indigenous birds under a scavenging system. It was also noted that scavenging flocks of exotic high-production birds (Rhode Island Red) were at slightly greater risk, perhaps as exotic birds are under more stress when kept under traditional management systems. We suggest that changes to the system of chicken production may alter the ecology and epidemiology of Campylobacter in the environment, chickens and people, which may drive emergence of new epidemiological patterns of disease. Further research is needed to determine the extent to which the current management intensification and the distribution programmes of exotic and/or improved indigenous birds may alter Campylobacter epidemiology, ecology and public health risk, before their widespread adoption.