Early pregnancy is characterised by adaptations in the maternal immune system to allow development of genetically disparate embryos. Immune tolerance is mediated by a subset of anti-inflammatory, homeostatic T cells known as regulatory (Treg) cells, and is influenced by maternal hormones, through mechanisms that are not well understood. We previously demonstrated a key role for P4 in regulating Treg cell abundance and phenotype in early pregnancy, using a mouse model of peri-implantation disruption in P4 signalling with the P4-receptor antagonist, RU486. Administration of low-dose RU486 (1 mg/kg) on day (d) 1.5 and 3.5 post-coitus (pc) to allogeneically mated C57Bl6 females caused a decreased Treg cell pool in mid-pregnancy, followed by a reduced pregnancy rate in late pregnancy (d18.5 pc) along with increased fetal resorptions. Here, we investigated the effect of transferring donor Treg cells to RU486-treated females. CD4+CD25+ Treg cells (or vehicle control) isolated from pregnant females (d11.5- d14.5 pc) were transferred intravenously on d3.5 pc to mated recipients treated with RU486. Strikingly, the reduced pregnancy rate was rescued in RU486-treated females administered Treg cells. Furthermore, Treg cell transfer to RU486-treated females restored fetal viability to levels comparable to control-treated females. In another group naïve/effector T cells (CD4+CD25-) were administered, and although pregnancy rate was improved, the number of viable pups per litter was reduced and fetal resorption was elevated compared to control-treated and Treg cell-treated females. This data shows that Treg cells can rescue pregnancy outcome in females where Treg cells are insufficient due to peri-implantation P4 signalling disruption. This demonstrates that P4 is a key determinant of Treg cells in pregnancy and that Treg cells are a key effector mechanism for P4 actions. Luteal phase and early pregnancy P4 is thus essential to prime Treg cells to drive a robust anti-inflammatory immune response necessary for optimal pregnancy success.