Mother-to-child transmission of HIV-1 via breastfeeding is responsible for nearly half of children newly infected with HIV. Although innate lymphoid cells (ILC) and natural killer (NK) cells are found throughout the oral mucosae, the effects of HIV/SHIV in these tissues are largely unknown. To better understand the mechanics of postnatal transmission we performed a comprehensive study of SIV/SHIV-infected infant rhesus macaques (RM) and tracked changes in frequency, trafficking, and function of ILC3 and NK cells using polychromatic flow cytometry and cell stimulation assays in colon, tonsil and oral lymph node samples. Infection led to a 3-fold depletion of ILC3 in the colon and an increase in NK cells in tonsils and oral lymph nodes. ILC3 and NK cells saw alterations in their trafficking repertoires as a result of infection, with increased expression of CD103 in colon NK cells and curtailment of CXCR3, and a significant decrease in 47 expression in colon ILC3. SPICE analyses revealed that ILC3 and NK cells displayed distinct functional profiles by tissue in nave samples. Infection perturbed these profiles, with a near total loss of IL-22 production in the tonsil and colon and increase in CD107a, IFN- and TNF- from ILC3, and increase in CD107a, MIP-1 and TNF- from NK cells. Collectively, these data reveal that lentiviurus infection alters the frequency, receptor repertoires, and functions of innate cells in the oral and gut mucosa of infants. Further study will be required to delineate the full extent that these changes have on oral and gut homeostasis, SHIV/SIV pathogenesis and oral opportunistic disease.Importance Vertical transmission of HIV from mother-to-child accounts for many of the new cases seen worldwide. To date, there is no vaccine to mitigate this transmission and limited research on the effects that lentiviral infection has on the innate immune system in oral tissues of infected children. To fill this knowledge gap, our lab studied infant rhesus macaques to evaluate how acute SIV/SHIV infections impacted ILC3 and NK cells; immune cells critical for mucosal homeostasis and antimicrobial defense. Our data revealed that SIV/SHIV infection led to a depletion of ILC3 and increase of NK cells, and a functional shift from homoestatic to multifunctional proinflammatory. Taken together, we describe how lentiviral infection perturbs the oral and gastrointestinal mucosae of infant macaques through alterations of resident innate immune cells giving rise to chronic inflammation and potentially exacerbating morbidity and mortality in children living with HIV.