In this study we report the first comprehensive metagenomic analysis of the prokaryotic and eukaryotic virome occupying luminal and mucosa-associated habitats along the entire length of the gastrointestinal tract (GIT) in two animal species, the domestic pig and rhesus macaque. The highest loads and diversity of bacteriophages are found in the lumen of the large intestine in both mammals. Mucosal samples contain much lower viral loads but a higher proportion of eukaryotic viruses. Parenchymal organs contained significant amounts of bacteriophages of gut origin, in addition to some eukaryotic viruses. GIT virome composition is both region- and species-specific with a strong separation between upper and lower gut. Nonetheless, certain viral and phage species are found ubiquitously from the oral cavity to the distal colon. Correlations between individual phages and their potential microbial hosts in the GIT are overwhelmingly positive, which confirms earlier concepts of the temperate-like life cycles of the majority of gut phages and a prevalence of the “piggyback-the-winner” ecological dynamics.