The human gut microbiota, a dense community of microorganisms residing in the gastrointestinal tract, assembles according to a defined developmental program during the first 1,000 days of life. Many chronic conditions are causally associated with impaired gut microbiome development, including childhood stunting. We developed a humanized mouse model of early life development providing the experimental framework to test phage-driven remodeling of the gut microbiota during this crucial period. After colonizing germ-free adult mice with fecal samples from 2 healthy infants and 1 toddler, mice were bred, and their pups studied until sexual maturity. Regular fecal sampling of breeders and pups allowed us to track colonization dynamics and vertical transmission of bacterial and viral taxa longitudinally. Fecal samples were processed for bacterial and viral metagenomics using a combination of amplicon, shotgun, and proximity-ligation (“Hi-C”) sequencing. Despite robust colonization of bacterial taxa in mice (44%), only 11% of viral operational taxonomic units (vOTUs) colonized these same mice, resulting in virome compositions distinct from those of the human donors. Over 95% of phage-host predictions were concordant at the phylum-, class-, and order-levels when comparing predictions from a recently developed bioinformatic tool to our proximity-ligation dataset. However, these prediction methods diverged significantly at the genus level, where there was only 67% concordance between approaches. Harnessing our multiple sequencing datasets and approaches, we also examined the impact of prophage induction in shaping virome composition in humanized mice, as a large proportion of vOTUs were detected in mice but not the original donor samples.