Bifidobacterium is a diverse genus of anaerobic, saccharolytic bacteria that colonize many animals, notably humans and other mammals. The presence of these bacteria in the gastrointestinal tract represents a potential coevolution between the gut microbiome and its mammalian host mediated by diet. To study the relationship between bifidobacterial gut symbionts and host nutrition, we analyzed the genome of two bifidobacteria strains isolated from the feces of a common marmoset (Callithrix jacchus), a primate species studied for its ability to subsist on host-indigestible carbohydrates. Whole genome sequencing identified these isolates as unique strains of Bifidobacterium callitrichos. All three strains, including these isolates and the previously described type strain, contain genes that may enable utilization of marmoset dietary substrates. These include genes predicted to contribute to galactose, arabinose, and trehalose metabolic pathways. In addition, significant genomic differences between strains suggest that bifidobacteria possess distinct roles in carbohydrate metabolism within the same host. Thus, bifidobacteria utilize dietary components specific to their host, both humans and non-human primates alike. Comparative genomics suggests conservation of possible coevolutionary relationships within the primate clade.