The human oral cavity is a hotspot of numerous, mostly unexplored, viruses that are important for maintaining oral health and microbiome homeostasis. Here, we analyzed 2,792 publicly available oral metagenomes and proposed the Oral Virus Database (OVD) comprising 48,425 nonredundant viral genomes (≥5 kbp). The OVD catalog substantially expanded the known phylogenetic diversity and host specificity of oral viruses, allowing for enhanced delineation of some underrepresented groups such as the predicted Saccharibacteria phages and jumbo viruses. Comparisons of the viral diversity and abundance of different oral cavity habitats suggested strong niche specialization of viromes within individuals. The virome variations in relation to host geography and properties were further uncovered, especially the age-dependent viral compositional signatures in saliva. Overall, the viral genome catalog describes the architecture and variability of the human oral virome, while offering new resources and insights for current and future studies.