Bovine genital campylobacteriosis (BGC) is a venereal disease caused by Campylobacter fetus that has a negative impact on animal reproduction. The bull is considered to be a symptomless carrier that spreads the disease agent to breeding cows, causing infertility and sporadic abortion. The study aims to estimate the prevalence, identify risk factors of Campylobacter fetus (C. fetus) infection and antimicrobial resistance pattern of the C. fetus isolates. A cross-sectional survey was conducted in Mymensingh district of Bangladesh. Bull smegma samples (single sample from each bull) were collected from 300 bulls from four farms and tested via culture, biochemical identification and finally 16S rRNA and cdtA gene-based molecular assays (PCR) for herd and animal-level prevalence estimation. Herd- and animal-level data on risk factors were collected from the farmers using a pretested questionnaire and analysed by univariable and multivariable logistic regression models with a p value of <0.05 was taken statistically significant for both analyses. Among the surveyed farms, 75% (95% CI: 19.4%-99.4%) were confirmed to have bulls infected with Campylobacter fetus at herd level. However, animal-level occurrence of C. fetus was estimated to be 8.7% (26/300) (95% CI: 5.7%-12.4%). Natural service increases the odds of campylobacteriosis 38.18 times (95% CI: 13.89-104.94) in comparison to artificial insemination for C. fetus infection in bulls. Significantly, half of the isolates (50%, n = 13) were identified to be multidrug resistant (MDR) for three to five antimicrobial agents. This study highlights the need to develop official guidelines for C. fetus control and prevention in Bangladesh including mandatory artificial insemination in reproductive cows and heifers, routine screening of breeding bulls for C. fetus free status.