Given the impact of viruses on microbial community composition and function, viruses have the potential to play a significant role in the fate of freshwater cyanobacterial harmful algal blooms (cHABs). Yet the role of viruses in cHABs remains poorly understood. We sought to address this knowledge gap with a metagenomic analysis of viruses of bloom-formingMicrocystis aeruginosaacross cHAB phases in the western basin of Lake Erie. Size-fractionation of the water allowed us to identify significant fraction-specific trends in viral diversity, which corresponded withMicrocystisgenetic diversity. Using a new machine-learning model, we predicted infections between viral and microbial host populations. We predicted hundreds of viral populations with infection histories includingMicrocystisand non-Microcystishosts, suggesting extensive interconnectivity and the potential for virus-mediated cross-species exchange of genetic material within cHABs communities. Infection predictions revealed a broad host range for Lake ErieMicrocystisviruses, challenging previous notions of "narrow" host-virus interactions in cHABs. Abundant viral genes belonging to predictedMicrocystisviruses revealed their potential role in key metabolic pathways and adaptation to environmental changes. We observed significant turnover of predictedMicrocystisvirus populations across time. Viral diversity was highest in the viral fraction and lowest in the colony-associated fraction, suggesting thatMicrocystiscolony formation and growth during cHABs leads to bottlenecks in viral diversity. These findings advance our understanding of uncultivatedMicrocystisvirus diversity, their potential effects on host metabolism, potential influence on species interactions, and potential coevolutionary processes between microbial hosts and their viral predators withinMicrocystis-dominated cHABs.