The Streptococcus bovis/Streptococcus equinus complex (SBSEC) is a group of animal and human-derived commensal bacteria, found in the rumen and gastrointestinal tract. These fast-growing organisms can over-proliferate in the rumen of cattle when they transition too quickly from forage to high grain diets, such as those employed in the feedlot industry. SBSEC strains are also opportunistic pathogens impacting on the health of ruminant livestock, having been associated with mastitis in dairy cattle and laminitis in cattle and horses. A pan-genome, incorporating the complete bacterial genome sequences of 39 predominantly livestock-derived SBSEC isolates (representing S. bovis, S. equinus, S. henryi, and S. gallolyticus) was developed. This pan-genome enabled the mechanisms which may contribute to the over-proliferation of these organisms within the rumen to be identified, including (a) compounds for inhibiting the growth of other microbes (bacteriocins), and (b) a wide variety of carbohydrate-degrading enzymes which enable these organisms to rapidly utilize high grain diets. The majority of SBSEC examined possessed genes coding for enzymes classified within eight glycosyl hydrolase families, capable of breaking down complex plant carbohydrates. The bacteriocin genes identified were primarily bacteriocin class II lantibiotics, however strain-specific bacteriocins were also noted. The identification of restriction-modification and CRISPR/cas systems also provided insights into how these organisms may defend themselves against phage infection. Despite the presence of these defense systems, 22 prophage-associated sequences, encoding a sufficient complement of phage genes to be designated as “intact” prophages, were identified within the pan-genome. Further examination of 13 S. equinus strains using proteomics and TEM, showed that at least three of these prophages produced intact phage particles. The establishment of an open, SBSEC pan-genome has therefore provided novel insights the extent of diversity, or lack thereof, found within gut-associated SBSEC isolates sourced from livestock around the globe.