Bacteriophages are important drivers of microbial ecosystems, but their influence and dynamics in terrestrial biomes remain poorly understood compared to aquatic and host-associated systems. To investigate this, we analyzed shotgun metagenomics datasets from ten compost-derived microbial communities propagated over 48 weeks. We found that the communities clustered into two distinct types consisting of hundreds of microbial genera, and in one community type identified Theomophage, a lytic bacteriophage representing a new Schitoviridae subfamily, which accounted for up to 74.3% of the total community metagenome, indicating massive viral outbreaks. We tracked molecular evolution of Theomophage and found that isolated communities were dominated by a single strain that showed little molecular evolution during outbreaks. However, when experimental manipulation allowed phages to migrate between communities, we observed transient coexistence of strains followed by genomic recombination that underpinned replacement of the ancestral strains. Additionally, when Theomophage colonized mesocosms where it was originally absent, new mutations evolved that fixed and spread to other communities. Our study describes the largest bacteriophage outbreak reported to date and reveals the spatial and temporal scales at which terrestrial bacteriophage microdiversity evolves. It also demonstrates that mixing of viral communities, which may be frequent in natural systems, promotes rapid bacteriophage evolution.