Brucellosis is a worldwide zoonosis with important public health, animal health and economic implications.Brucella melitensis, commonly associated with small ruminants, is an emerging bovine pathogen in dairy farms. We analysed allB. melitensisoutbreaks affecting dairy farms in Israel since 2006, combining traditional and genomic epidemiology to explore the public health implications of this One Health challenge. Whole-genome sequencing was applied to bovine and related humanB. melitensisisolates from dairy farm outbreaks. cgMLST-based and SNP-based typing was integrated with epidemiological and investigation data. A secondary analysis combining the bovine-human isolates with endemic human isolates from southern Israel was performed. A total of 92 isolates from dairy cows and related human cases originating from 18 epidemiological clusters were analysed. Most genomic and epi-clusters were congruent, but sequencing showed relatedness between apparently unrelated farm outbreaks. Nine secondary human infections were also genomically confirmed. The bovine-human cohort appeared intermixed with 126 endemic human isolates in southern Israel. We show a persistent and widespread circulation ofB. melitensisin dairy farms in Israel with secondary occupational human infection. The genomic epidemiology also uncovered cryptic connections between outbreaks. A regional connection between bovine and endemic human brucellosis cases points to a common reservoir, most probably local small ruminant herds. Control of humans and bovine brucellosis is inseparable. Epidemiological and microbiological surveillance and implementation of control measures across the entire range of farm animals is needed to mitigate this public health challenge.