Protein kinase C-θ (PKC-θ) is essential for the activation of T cells in autoimmune disorders, but not in viral infections. To study the role of PKC-θ in bacterial infections, PKC-θ−/− and wild-type mice were infected with Listeria monocytogenes (LM). In primary and secondary listeriosis, the numbers of LM-specific CD8 and CD4 T cells were drastically reduced in PKC-θ−/− mice, resulting in increased CFUs in spleen and liver of both PKC-θ−/− C57BL/6 and BALB/c mice. Furthermore, immunization with peptide-loaded wild-type dendritic cells induced LM-specific CD4 and CD8 T cells in wild-type but not in PKC-θ−/− mice. In listeriosis, transfer of wild-type T cells into PKC-θ−/− mice resulted in a normal control of Listeria, and, additionally, a selective expression of PKC-θ in LM-specific T cells was sufficient to drive a normal proliferation and survival of these T cells in LM-infected PKC-θ−/− recipients, illustrating a cell-autonomous function of PKC-θ in LM-specific T cells. Conversely, adoptively transferred PKC-θ−/− T cells were partially rescued from cell death and proliferated in LM-infected wild-type recipients, demonstrating that a PKC-θ deficiency of LM-specific T cells can be partially compensated for by a wild-type environment. Additionally, in vitro experiments showed that only the addition of IL-2, but not an inhibition of caspase-3, induced proliferation and prevented death of PKC-θ−/− T cells stimulated with LM-infected wild-type dendritic cells, further demonstrating that the impaired proliferation and survival of PKC-θ−/− T cells in listeriosis is not intrinsically fixed and can be experimentally improved.