Age-associated changes in the functionality of CD4 T cells have been linked to both declined immunity and chronic inflammation. However, a detailed characterization of CD4 T cell phenotypes, which may explain these dysregulated functional properties, is lacking. Here, we used single-cell RNA sequencing and multidimensional protein analyses to profile thousands of CD4 T cells obtained from young and old mice. We found that the landscape of CD4 T cell subsets is markedly different between young and old mice, such that three cell subsets, including exhausted, cytotoxic, and activated regulatory T cells (aTregs), appear rarely in young mice and gradually accumulate with age. Most unexpected were the cytotoxic CD4 T cells and aTregs exhibiting extreme pro- and anti-inflammatory phenotypes, respectively. These findings provide a comprehensive view of the dynamic reorganization of the CD4 T cell milieu with age and illuminate dominant cell subsets associated with declined immunity and chronic inflammation, suggesting new therapeutic avenues for age-related diseases.