Abstract Giant viruses can control their eukaryotic host populations, shaping the ecology and evolution of aquatic microbial communities. Understanding the impact of the viruses’ own parasites, the virophages, on the control of microbial communities remains a challenge. Most virophages have two modes of infection. They can exist as free particles coinfecting host cells together with the virus, where they replicate while inhibiting viral replication. Virophages can also integrate into the host genome, replicate through host cell division and remain dormant until the host is infected with a virus, leading to virophage reactivation and replication without inhibiting viral replication. Both infection modes (reactivation vs. coinfection) occur within host-virus-virophage communities, and their relative contributions are expected to be dynamic and context dependent. The consequences of this dynamic regime for ecological and evolutionary dynamics remain unexplored. Here, we test whether and how the relative contribution of virophage infection modes influences the ecological dynamics of an experimental host-virus-virophage system and the evolutionary responses of the virophage. We indirectly manipulated the level of virophage (Mavirus) integration into the host (Cafeteria burkhardae) in the presence of the giant Cafeteria roenbergensis virus. Communities with higher virophage integration were characterized by lower population densities and reduced fluctuations in host and virus populations, whereas virophage fluctuations were increased. The virophage evolved toward lower inhibition and higher replication, but the evolution of these traits was weaker with higher virophage integration. Our study shows that differences in the virophage infection modes contributes to the complex interplay between virophages, viruses and hosts.