Bacteriophages, the viruses that infect bacteria, are the most abundant biological entities on earth. Despite this, little is known about their ecology and community-level dynamics relative to their bacterial counterparts. Recent bioinformatics advances facilitate previously-infeasible viral community profiling from large-scale shotgun metagenomic and metatranscriptomic sequencing data, providing a new avenue to assess the impact of viral dynamics and function on the microbiome. To that end, we leveraged existing meta’omics datasets (i.e. HMP2) and developments in viral community profiling to identify bacteriophage determinants of microbial ecology and function. By integrating functional metagenomics with phage-host prediction, we provide evidence that promiscuous phage, i.e. those with a broad host range, are abundant in the enteric human microbiome and associate with microbiota functional shifts in a manner consistent with phage-mediated selection and transcriptomic response to phage infection. Moreover, we posit that phage promiscuity acts as an emergent property to constrain and stabilize microbiome community structure, specifically acting to prevent successful colonization of immigrating competitors to a phage’s primary bacterial host at the community level. Overall, this work highlights the active role bacteriophages play in shaping microbial communities, and provides a systems-level framework for determining viral drivers of microbial functions. Over the longer term, such efforts contribute to our basic understanding of the complex ecological dynamics driving microbial community stability and composition and allow optimal bacteriophage selection for precision control of the microbiome as a novel therapeutic intervention.