Bovine tuberculosis, caused by Mycobacterium bovis (M. bovis), is a globally distributed chronic disease of animals. The bacteria can be transmitted to humans via the consumption of unpasteurised (raw) milk, thus representing an important public health risk. To investigate the risk of zoonotic transmission of M. bovis via raw milk, this study systematically reviewed published studies to estimate the prevalence of M. bovis in on-farm bulk-tank milk (BTM) and individual cow's milk (IM) by meta-analysis. In total, 1,339 articles were identified through seven electronic databases and initially screened using titles and abstracts. The quality of 108 potentially relevant articles was assessed using full texts, and 67 articles comprising 83 studies (76 IM and 7 BTM), were included in the meta-analysis. The prevalence of M. bovis in IM and BTM was summarised according to the diagnostic test used, and the tuberculin skin test (TST) infection status of the individual cows (for IM) or herds (for BTM). Heterogeneity was quantified using the I-squared statistic. Prediction intervals (95% PIs) were also estimated. For IM, the overall prevalence was summarised at 5% (95%CI: 3%-7%). In TST positive cows, prevalence was summarised at 8% (95%CI: 4%-13%). For BTM, the overall prevalence independent of individual herd TST infection status was summarised at 5% (95%CI: 0%-21%). There was considerable heterogeneity evident among the included studies, while PIs were also wide. Inconsistency in the quality of reporting was also observed resulting in missing information, such as the TST infection status of the individual animal/herd. No study reported the number of M. bovis bacteria in test-positive milk samples. Several studies reported the detection of M. tuberculosis and M. africanum in milk. Despite international efforts to control tuberculosis, this study highlights the risk of zoonotic transmission of M. bovis via unpasteurised milk and dairy products made using raw milk.