γδ T cells show preferential homing that is characterized by biased TCR repertoire at different anatomical locations. The processes that regulate this compartmentalization are largely unknown. A model that allows repeated multiple sample procurement under different conditions and enables with relatively straightforward extrapolation to a human situation will facilitate our understanding. The peripheral blood Vγ2 T cell population is the best-characterized human γδ T cell subset. To determine its diversity at multiple immunocompartments matching blood, colon, and vagina samples from rhesus macaques were investigated. Four joining segments used in Vγ2-Jγ transcripts were identified, including one segment with no human counterpart. Like in humans, the rhesus peripheral blood Vγ2 TCR repertoire was limited and contained common sequences that were shared by genetically heterogeneous animals. Furthermore, this subset comprised several phylogenetically conserved Vγ2 complementarity-determining region 3 (CDR3) motifs between rhesus and humans. Common sequences were also found within the colon and vagina of the same animal, and within the peripheral blood and intestine of different unrelated animals. These results validate rhesus macaques as a useful model for γδ TCR repertoire and homing studies. Moreover, they provide evidence that the concept of limited but overlapping Vγ TCR repertoire between unrelated individuals can be extended including the mucosa of the digestive and reproductive tract.