Although there are many reports on the splenic (systemic) T cell response after Toxoplasma gondii infection, little information is available regarding the local T cell responses of peritoneal exudate cells (PEC) and gut intraepithelial lymphocytes (IEL) following peroral infection with bradyzoites. Mice were infected with 40 cysts of the 76K strain of T. gondii, and then sacrificed at days 0, 1, 4, 7 and 10 postinfection (PI). The cellular composition and T cell responses of PEC and IEL were analyzed. The total number of PEC and IEL per mouse increased after infection, but the ratio of increase was higher in IEL. Lymphocytes were the major component of both PEC and IEL. The relative percentages of PEC macrophages and neutrophils/eosinophils increased significantly at day 1 and 4 PI, whereas those of IEL did not change significantly. The percentage of PEC NK1.1 and γδ T cells peaked at day 4 PI (p < 0.0001), and CD4 and CD8α T cells increased continuously after infection. The percentages of IEL CD8α and γδ T cells decreased slightly at first, and then increased. CD4 and NK1.1 T cells of IEL did not change significantly after infection. IFN-γ-producing PEC NK1.1 T cells increased significantly from day 1 PI, but the other T cell subsets produced IFN-γ abundantly thereafter. The proportion of IEL IFN-γ-producing CD8α and γδ T cells increased significantly after infection, while IEL NK1.1 T cells had similar IFN-γ production patterns. Taken together, CD4 T cells were the major phenotype and the important IFN-γ-producing T cell subsets in PEC after oral infection with T. gondii, whereas CD8α T cells had these roles in IEL. These results suggest that PEC and IEL comprise different cell differentials and T cell responses, and according to infection route these factors may contribute to the different cellular immune responses.