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Camelpox is endemic in most camel rearing regions of the world, causing significant economic losses. However, its epidemiology is not extensively investigated. We conducted a cross sectional seroprevalence study of camelpox in Amibara and Awash Fentale districts in Afar region of Ethiopia from November 2014 to May 2015. In addition, participatory epidemiology (PE) was conducted to identify seasonal occurrence of the disease in the study districts. Blood samples were collected from 384 dromedary camels from 31 herds distributed in five pastoral associations (PAs) in the two districts. Serum samples were separated from the blood samples and tested for the presence of viral antibodies using virus neutralization test. Seroprevalence data were analyzed using multilevel mixed effects logistic regression models accounting for the 4-level hierarchical data structure (camels nested in herds-herds in PA, and PA in district). For the participatory data, Kendall’s coefficient of concordance was used to assess agreements between the informants in identifying seasonal occurrences of the top five camel diseases. Camelpox antibodies were detected in 19.3% of camels (n = 384), 81% of herds (n = 31), and in all five PAs from the two districts in the Gabi Rasu zone of Afar region, Ethiopia. The seroprevalence did not significantly vary between herds, PAs or districts suggesting the widespread occurrence of the disease. Estimated age stratified basic reproduction number (R0) was 1.25 (95% CI: 0.62–2.19). Camelpox was identified as one of the top five common camel diseases in the area. The widespread occurrence of the disease can be attributed mainly to the commingling of camels from many herds during seasonal migration in search of feed and water, a practice very common under pastoral production systems. Although the PE informants indicated the clinical disease to be more common in young animals, seropositivity was higher in older animals. Camelpox commonly occurs during the minor and major rainy seasons. In conclusion, camelpox is found to be endemic in Afar pastoral region with sporadic outbreaks occurring during rainy seasons. Vaccination and improved camel management practices particularly during the high-risk period can be viable strategies to reduce the burden of the disease.