Freshwater bloom-forming cyanobacteria densely grow in the aquatic environments, leading to an increase in the viral-contact rate. They possess numerous antiviral genes, as well as cell differentiation- and physiological performance-related genes, owing to genome expansion. Their genomic features and unique lifestyles suggest that they coexist with cyanoviruses in ways different from marine cyanobacteria. Furthermore, genome contents of isolated freshwater bloom-forming cyanobacterial viruses have little in common with those of marine cyanoviruses studied to date. They lack the marine cyanoviral hallmark genes that sustain photosynthetic activity and redirect host metabolism to viral reproduction; therefore, they are predicted to share metabolisms and precursor pools with host cyanobacteria to ensure efficient viral reproduction and avoid nutrient deficiencies and antiviral response. Additionally, cyanovirus-cyanobacteria coexistence strategies may change as bloom density increases. Diverse genotypic populations of cyanoviruses and hosts coexist and fluctuate under high viral-contact rate conditions, leading to their rapid coevolution through antiviral responses. The ancestral and newly evolved genotypes coexist, thereby expanding the diversity levels of host and viral populations. Bottleneck events occurring due to season-related decreases in bloom-forming species abundance provide each genotype within cyanobacterial population an equal chance to increase in prevalence during the next bloom and enhance further diversification.