Background: Toxoplasma gondii（T. gondii） infection during pregnancy can lead to fetal defect or congenital complications. The inhibitory molecule B7-H4 expressed on decidual macrophage (dMφ) exerted important role in maternal-fetal tolerance. However, the effect of B7-H4 on the function of dMφ during T. gondii infection remains unclear. Methods: In the present study, the change of B7-H4 expression on dMφ after T. gondii infection were explored in vivo and in vitro. B7-H4-/- pregnant mice and purified primary human dMφ treated by B7-H4 neutralizing antibody were used to explore the role of B7-H4 signaling on regulating the membrane molecules, arginine metabolic enzymes synthesis, and cytokines production of dMφ with T. gondii infection. Also adoptive transfer of dMφ from WT pregnant mice or B7-H4-/- pregnant mice to infected B7-H4-/- pregnant mice were used to examine the effect of B7-H4 on adverse pregnancy outcomes induced by T. gondii infection. Results: Our results illustrated that B7-H4-/- pregnant mice infected by T. gondii displayed poorer pregnancy outcomes than those of the wild-type counterparts. B7-H4 expression on dMφ significantly decreased after T. gondii infection, which further resulted in the polarization of dMφ from M2 toward M1 phenotype by changing the expression of membrane molecules (CD80, CD86, CD163, CD206), arginine metabolic enzymes (Arg-1, iNOS) synthesis, and cytokines (IL-10, TNF-α) production. Also, we found that the B7-H4 down-regulation after T. gondii infection increased iNOS and TNF-α expression through JAK2/STAT1 signaling pathway. Besides, adoptive transfer of dMφ from WT pregnant mice donor rather than B7-H4-/- pregnant mice donor could improve adverse pregnancy outcomes induced by T. gondii infection. Conclusions: The results demonstrated that the downregulation of B7-H4 induced by T. gondii infection leaded to the dysfunction of decidual macrophages and contributed to abnormal pregnancy outcomes. Moreover, adoptive transfer of B7-H4+dMφ could improve adverse pregnancy outcomes induced by T. gondii infection.