The extent of infection and rate of pathogen clearance are thought to determine both the magnitude of antigen-specific CD8⁺ T cell expansion and the ensuing contraction to a stable number of memory cells. We show that CD8⁺ T cell expansion after Listeria monocytogenes infection was primarily dependent on the initial infection dose or amount of antigen displayed, and was also influenced by the rate of pathogen clearance. However, the onset and kinetics of CD8⁺ T cell contraction after L. monocytogenes and lymphocytic choriomeningitis virus infections were independent of the magnitude of expansion, dose and duration of infection or amount of antigen displayed. Thus, major features of antigen-specific CD8⁺ T cell homeostasis, including the contraction phase of an immune response, may be programmed early after infection.