The prototypic crAssphage (Carjivirus communis) is an abundant, prevalent, and persistent human gut bacteriophage, yet it remains uncultured and its lifestyle uncharacterized. C. communis does not readily plaque, suggesting a largely non-lytic lifestyle. Here, we find that C. communis is a linear phage-plasmid that stably persists extrachromosomally within its host. Plasmid and phage-related genes are transcribed, and multiple putative replication origins may initiate replication for multiple lifestyles and genome conformations, including both circular and linear formations. Leveraging these findings, we use a plaque-free culturing approach to measure C. communis replication on prevalent gut bacteria, notably Phocaeicola vulgatus, P. dorei, and Bacteroides stercoris, revealing a broad host range. C. communis persists without causing major cell lysis events or integrating into host chromosomes. Taken together, C. communis' ability to switch between phage and plasmid lifestyles within a wide range of hosts may contribute to its widespread presence in human gut microbiomes.