Background: Polinton-like viruses (PLVs) are diverse eukaryotic DNA viral elements (14-40 kbp) that often undergo significant expansion within protist genomes through repeated insertion events. Emerging evidence indicates they function as antiviral defense systems in protists, reducing the progeny yield of their infecting giant viruses (phylum Nucleocytoviricota) and influencing the population dynamics and evolution of both viruses and their hosts. While many PLVs have been identified within the genomes of sequenced protists, most were recovered from metagenomic data. Even with the large number of PLVs identified from metagenomic data, their host-virus linkages remain unknown owing to the scarcity of ecologically relevant protist genomes. Additionally, the extent of PLV diversification within abundant freshwater taxa remains undetermined. In order to tackle these questions, high-quality genomes of abundant and representative taxa that bridge genomic and metagenomic PLVs are necessary. In this regard, Cryptophytes, that are among the most widely distributed, abundant organisms in freshwaters and have remained largely out of bounds of genomic and metagenomic approaches, are ideal candidates for investigating the diversification of such viral elements both in cellular and environmental context. Results: We leveraged long-read sequencing to recover large (200-600 Mb), high quality and highly repetitive (>60%) genomes of representative freshwater and marine photosynthetic cryptophytes. We uncovered over one thousand complete PLVs within these genomes revealing vast lineage-specific expansions, particularly in the common freshwater cryptophyte Rhodomonas lacustris. By combining deep sequence homology annotation with biological network analyses, we discern well-defined PLV groups defined by characteristic gene-sharing patterns and the use of distinct strategies for replication and integration within host genomes. Finally, the PLVs recovered from these cryptophyte genomes also allow us to assign host-virus linkages in environmental sequencing data. Conclusions: Our findings provide a primer for understanding the evolutionary history, gene content, modes of replication and infection strategies of cryptophyte PLVs, with special emphasis on their expansion as endogenous viral elements (EVEs) in freshwater bloom-forming Rhodomonas lacustris.