Bacteriophages like Mu are able to integrate their genome almost randomly in the host chromosome, replicate their DNA by transposition and carry segments of host DNA attached at both genome termini on the viral particles. Whereas these phages have been described in several bacteria as rare elements, in P. aeruginosa they seem to be common and have been classified into the D3112virus genera. Since several representatives of these phages have been sequenced, in this work we present the pangenome analysis of the group by comparing 40 genomes from phages and prophages reported in databases and isolated around the globe in order to study their genomic diversity and how they impact their host's genome. Our functional annotation was enriched by mass spectrometry analysis of the virion of one representative, which allowed us to identify eight structural proteins previously annotated as hypothetical. Based on the comparative analysis we determined a core component comprising 47 ORFs which represents most of the genome and encodes essential functions for the phages. The remaining ORFs, which are different for each genome, are encoded in specific loci defined as Regions of Genomic Plasticity and correspond to the accessory component of the group. Based on the inferred and known functions for some of the accessory genes, they appear to confer selective advantages for the phage survival under particular host conditions, as is the case of the anti-CRISPR genes which have been reported in these phages. Besides the sequence divergence observed on the core genome, the main source of diversity in these genomes resides on the accessory component, implying their impact on the gene diversity of their host also. Thus, our observations extend the concept of “pangenome” to the group of D3112virus, not only in the genome architecture, but also in their functional and evolutionary implications for phage biology.