Lactococcus lactis is the most widely employed starter bacterium in dairy fermentations globally. Lactococcal phages present one of the most significant challenges to such dairy fermentation processes and are, therefore, the subject of intense research focus in recent years. The lactococcal P335 phages, which are currently classified into four sub-groups, are the second most frequently isolated phage group in the dairy industrial context. Here, we describe the isolation and comparative genomic analysis of 17 novel P335 group phages. Focused analysis of the genomic region of P335 phages encoding the so-called “baseplate” or adhesion device was undertaken. This analysis revealed a significant sequence divergence within RBP sequences, reflecting their unique interactions with the host and a preference for A-CWPS. Additionally, some lactococcal phages have previously been shown to require calcium for plaque formation and in this study, it was observed that the sub-group IV P335 phages are specific in their requirement for calcium for plaque formation. Finally, antibody neutralization assays were employed to identify the RBP of sub-group III P335 phages LC3 and Dub35A and the Group IV phage Q33. The implications of genomic architecture of lactococcal P335 phages on serving as a general model for Siphoviridae phages are discussed.