We used a sensitive method based on tetramers of peptide and major histocompatibility complex II (pMHCII) to determine whether CD4⁺ memory T cells resemble the T helper type 1 (T_H1) and interleukin 17 (IL-17)-producing T helper (T_H17) subsets described in vitro. Intravenous or intranasal infection with Listeria monocytogenes induced pMHCII-specific CD4⁺ naive T cells to proliferate and produce effector cells, about 10% of which resembled T_H1 or T_H17 cells, respectively. T_H1 cells were also present among the memory cells that survived 3 months after infection, whereas T_H17 cells disappeared. The short lifespan of T_H17 cells was associated with small amounts of the antiapoptotic protein Bcl-2, the IL-15 receptor and the receptor CD27, and little homeostatic proliferation. These results suggest that T_H1 cells induced by intravenous infection are more efficient at entering the memory pool than are T_H17 cells induced by intranasal infection.