Mesophilic starter cultures rely on the activity of lactic acid bacteria such as Lactococcus lactis and Lactococcus cremoris for the acidification of milk. This biotechnological process can be affected by bacteriophage infection of bacterial starter strains resulting in failed or delayed fermentations. The majority of studied lactococcal phages commence infection with the binding of a tail-associated receptor binding protein (RBP) to a host surface-exposed cell wall polysaccharide (CWPS). In the present study, phage prevalence and phage diversity in whey samples originating from fermentations performed in various European countries and employing mesophilic undefined, complex starter cultures were investigated using phageome analysis. The diversity and prevalence of Skunavirus RBP genotypes of phageome-identified Skunavirus contigs was evaluated. Through sequence and structural analysis of available Skunavirus RBP sequences, the previous Skunavirus RBP grouping system (group I-V) was refined and expanded to now encompass eleven groups and several subgroups. Through the generation of His-tagged GFP-RBP fusion proteins, attempts were made to link specific RBP (sub)groups to the CWPS type of the corresponding host(s) of phages encoding a given RBP. These findings vastly improve our knowledge on lactococcal Skunavirus RBP diversity and their specificity towards CWPS receptor structures, thereby improving the predictability of fermentation outcomes and robustness of starter culture rotations or blends. In addition, this study demonstrates the increasing genetic and structural diversity exhibited by both host surface-exposed receptors and phage-encoded RBP through the co-evolution of bacteria and their infecting phages.