Bacteriophages are a persistent problem in dairy plants. Streptococcus thermophilus is a component of thermophilic starter cultures used for cheese and yoghurt production. In this study, a multiplex PCR method was adapted to identify, in a single reaction, all known S. thermophilus phage groups. The method was compared with the previously published multiplex PCR typing method and showed higher specificity for classifying purified phage isolates. Three new representatives of phage group 5093, which were discovered with the developed PCR method, were genome sequenced and the genomes were compared with those available in GenBank. A validation of the two typing methods performed with whey revealed limitations of multiplex PCR assays when applied for the detection of phages in dairy samples. This study established an improved multiplex PCR method for classifying purified S. thermophilus phages, and expanded the genetic information of group 5093, both important steps to control phage infections in dairies.