The maternal immune response is central to the timing of parturition and labour, but the underpinning mechanisms are ill-defined. Increasingly, evidence points to the quality of immune adaptation in early pregnancy as a driver of pregnancy tolerance and protection from late gestation adverse outcomes. We recently demonstrated luteal phase progesterone (P4) signalling is a central regulator of the maternal CD4+ T cell response in pregnancy. In a model of T cell dysfunction caused by impaired luteal phase P4 signalling, low-dose P4 antagonist RU486 (1 mg/kg) administered on 1.5 and 3.5 dpc led to poor pregnancy viability and fetal growth restriction. Transferring regulatory T (Treg) cells to RU486-treated mice showed that P4-induced Treg cells are necessary for healthy pregnancy and fetal growth. Unexpectedly, a parturition defect was also revealed, as RU486-treated dams delivered ~24 hours later than controls (P<0.0001; 18.8 vs 19.7 dpc) and failed to undergo serum P4 decline at 18.5 dpc (P<0.05 vs control), raising the question of whether T cells induced by P4 are involved in regulating parturition. Here, we investigated this by adoptively transferring CD4+CD25+ Treg cells or CD4+CD25- T conventional (Tconv) cells into RU486-treated mice on 3.5 dpc. Interestingly, transfer of Tconv cells (P=NS vs control), but not Treg cells (P<0.05 vs control), restored the timing of birth following P4 signalling disruption. Furthermore, there was a strong inverse correlation (r= -0.81) between plasma P4 concentration on 18.5 dpc and number of viable fetuses, suggesting that fetal antigen-driven T cell responses might promote luteal regression preceding parturition. These data demonstrate that a distinct subset of CD4+ T cells mediates events required for on-time parturition, and generation of this cell population depends on sufficient luteal phase P4 at the outset of pregnancy. These findings provide insight relevant to the pathophysiology of prolonged pregnancy and stillbirth risk in women.