Bacteriophage, viruses that infect bacteria, have great specificity for their bacterial hosts at the strain and species level. However, the relationship between the phageome and associated bacterial population dynamics is unclear. Here, we generated a computational pipeline to identify sequences associated with bacteriophage and their bacterial hosts in cell-free DNA (cfDNA) from plasma samples. Analysis of two independent cohorts, including a Stanford Cohort of 62 septic patients and 10 controls and the SeqStudy cohort of 224 septic patients and 167 controls, reveales a circulating phageome in the plasma of all sampled individuals. Moreover, infection is associated with overrepresentation of pathogen-specific phages, allowing for identification of bacterial pathogens. We find that information on phage diversity enables identification of the bacteria that produced these phages, including pathovariant strains of Escherichia coli. Phage sequences can likewise be used to distinguish between closely-related bacterial species such as Staphylococcus aureus, a frequent pathogen, and coagulase-negative Staphylococcus, a frequent contaminants such as. Phage cfDNA may have utility in studying bacterial infections.