The large-scale and high-intensity application of Streptococcus thermophilus species in milk fermentation processes is associated with a persistent threat of (bacterio)phage infection. Phage infection of starter cultures may cause inconsistent, slow or even failed fermentations with consequent diminished product quality and/or output. The phage life cycle commences with the recognition of, and binding to, a specific host-encoded and surface-exposed receptor, which in the case of S. thermophilus can be the rhamnose-glucose polysaccharide (RGP; specified by the rgp gene cluster) or exopolysaccharide (EPS; specified by the eps gene cluster). The genomic diversity of 23 S . thermophilus strains isolated from unpasteurized dairy products was evaluated, including a detailed analysis of the rgp and eps loci. In the present study, five novel eps genotypes were identified while variations of currently recognized rgp gene cluster types were also observed. Furthermore, the diversity of rgp genotypes amongst retrieved isolates positively correlated with phage diversity based on phageome analysis of eight representative dairy products. Our findings therefore substantially expand our knowledge on S. thermophilus’ strain and phage diversity in (artisanal) dairy products and highlight the merit of phageome analysis of artisanal and traditional fermented foods as a sensitive marker of dominant microbiota involved in the fermentation.