For many years Streptococcus agalactiae has been considered an obligate intramammary and strictly contagious pathogen in dairy cattle. However, recent reports of S. agalactiae isolation from extramammary sources have contradicted that premise. To gain further insight into the epidemiology of S. agalactiae infection in cattle, we examined its distribution and heterogeneity of strains in bovine milk, bovine feces, and the environment in Colombian dairy farms. First, a longitudinal study was conducted at herd level in 152 dairy herds. Bulk tank milk samples from each herd where collected twice a month for six months. A follow-up study with a cross sectional design at the cow level was conducted in a subset of 25 farms positive for S. agalactiae. Cow-level milk samples from 1712 lactatting cows and 1545 rectal samples were collected, as well as 120 environmental samples. Samples were used for S. agalactiae detection and genotyping using Multi Locus Sequence Typing. Results showed sporadic rather than repeated isolation of S. agalactiae from bulk tank milk in 40% of the positive herds, challenging the idea that S. agalactiae is a highly contagious pathogen causing chronic infections. S. agalactiae was isolated from rectal or environmental samples in 32% and 12% of cross-sectional study farms, respectively, demonstrating that the bacteria can survive in extramammary sources and that S. agalactiae is not an obligate intramammary pathogen. The same strain was isolated from rectal and bulk tank milk samples in eight farms, suggesting that fecal shedding is frequent, and contributes to the presence of S. agalactiae in bulk tank. High within-herd heterogeneity of strains was found, which is distinct from the situation in developed dairy industries. These new epidemiological findings should be considered to adjust surveillance and control recommendations for S. agalactiae.