Campylobacteriosis is an infectious zoonotic disease caused by the genus Campylobacter. The disease is transmitted from animals to humans predominantly through the consumption of contaminated food and water. However, the lack of information on the status of Campylobacter makes it difficult to quantify the role of camel meat in the dissemination of the pathogen. A cross-sectional study was conducted from June 2022 to August 2023 to investigate the occurrence of Campylobacter and associated risk factors and to determine the antimicrobial susceptibility profiles of Campylobacter species from camels slaughtered at municipal abattoirs in the towns of Harar, Babile, Jigjiga and Dire Dawa in eastern Ethiopia. A total of 324 (146 carcass swabs, 146 camel feces and 32 abattoir environmental swab samples) were collected and analyzed using TaqMan real-time PCR and culture techniques following standard procedures. In addition, antimicrobial susceptibility tests were performed using the disk diffusion method for eight antimicrobial agents according to the Clinical Laboratory Standards Institute. The overall prevalence of Campylobacter was 7.7%. Campylobacter was more frequently detected from carcasses and surface contact environmental swabs. We isolated Campylobacter at the genus level from approximately half of the PCR-positive samples, representing 54.2% (13 out of 24) of the total. The isolation levels of C. jejuni and C. coli were also 5.56% and 2.2%, respectively, which varied significantly (p = 0.037) based on sample type and site. The odds of occurrence of C. jejuni in samples collected from abattoir environments was 7.52 times greater than those in carcass and fecal samples. We detected resistance to chloramphenicol (78.6%), followed by amoxicillin (71.4%). However, 93%, 78.6%, and 71.4% of the isolates were susceptible to ceftriaxone, ciprofloxacin, and nalidixic acid, respectively. Multidrug resistance (MDR) was detected in 60% of the isolates. Of these MDR isolates, 9 (75%) were C. jejuni and 3 (25%) were C. coli. This study revealed that a considerable proportion of multidrug-resistant Campylobacter species circulate in both camel meat and abattoir environments. This indicates possible carcass cross-contamination by Campylobacter during slaughtering that can pose a threat to humans and limit therapeutic options, which could be prevented by applying good hygienic practices at abattoirs. Therefore, abattoir workers need to be aware of abattoir hygienic standard operating procedures. Regular coordinated actions should be implemented for the rational use of veterinary and medical drugs at the national level, together with training and awareness of hygienic practices.