HIV disease progression appears to be driven by high levels of immune activation. Given observations that fetal exposure to infectious pathogens in utero can result in reduced immune responses, or tolerance, to those pathogens postnatally, we hypothesized that fetal exposure to HIV may tolerize the fetus to the virus, thus reducing damage caused by immune activation if infected later in life. To test this hypothesis, fetal rhesus macaques (Macaca mulatta) were injected with the attenuated virus SIVmac1A11 in utero and then challenged with pathogenic SIVmac239 one year after birth. SIVmac1A11-injected animals had significantly reduced plasma RNA viral loads (p<0.02) up to 35 weeks post-infection. Generalized estimating equations (GEE) analysis was performed to identify immunologic and clinical measurements significantly associated with plasma RNA viral load. A positive association was observed with the proportion of CD8+ T cells expressing the transcription factor, FoxP3, and the proportion of CD4+ T cells producing the lymphoproliferative cytokine, IL-2, while an inverse relationship was found with the levels of circulating CD4+ and CD8+ T cells expressing intermediate levels of the proliferation marker, Ki-67. Further analyses demonstrated that animals exposed to SIV in utero appeared to have enhanced SIV-specific cellular immune responses, expressed lower levels of the exhaustion marker, PD-1, on CD8+ T cells, and had more circulating Th17 cells when compared to controls. While the development of tolerance was not demonstrated, these data suggest that rhesus monkeys exposed to SIVmac1A11 in utero had distinct immune responses associated with the control of viral replication after postnatal challenge.