<jats:p> Phages are important in aquatic ecosystems as they influence their microbial hosts through lysis, gene transfer, transcriptional regulation, and expression of phage metabolic genes. Still, there is limited knowledge of how phages interact with their hosts, especially at fine scales. Here, a <jats:italic>Rheinheimera</jats:italic> phage-host system constituting highly similar phages infecting one host strain is presented. This relatively limited diversity has previously been seen only when smaller numbers of phages have been isolated and points toward ecological constraints affecting the <jats:italic>Rheinheimera</jats:italic> phage diversity. The variation of metabolic genes among the species points toward various fitness advantages, opening up possibilities for future hypothesis testing. Phage-host dynamics monitored over several years point toward recurring “kill-the-winner” oscillations and an ecological niche fulfilled by this system in the Baltic Sea. Identifying and quantifying ecological dynamics of such phage-host model systems <jats:italic>in situ</jats:italic> allow us to understand and study the influence of phages on aquatic ecosystems. </jats:p>