Streptococcus thermophilus ASCC 1275 (ST 1275), a typical dairy starter bacterium, yields the highest known amount (~1,000 mg/L) of exopolysaccharide (EPS) in milk among the species of S. thermophilus. The addition of this starter in milk fermentation exhibited texture modifying properties for fermented dairy foods such as yogurt and cheese in the presence of EPS as its important metabolite. In this genomic study, a novel eps gene cluster for EPS assembly of repeating unit has been reported. It contains two-pair epsC-epsD genes which are assigned to determine the chain length of EPS. This also suggests this organism produces two types of EPSs - capsular and ropy EPS, as observed in our previous studies. Additionally, ST 1275 appears to exhibit effective proteolysis system and sophisticated stress response systems to stressful conditions, and has the highest number of four separate CRISPR/Cas loci. These features may be conducive to milk adaptation of this starter and against undesirable bacteriophage infections which leads to failure of milk fermentation. Insights into the genome of ST 1275 suggest that this strain may be a model high EPS-producing dairy starter.