In spite of thymic involution early in life, the numbers of naive CD4⁺ T cells only slowly decline in ageing humans implying peripheral post‐thymic naive CD4⁺ T cell expansion. This proliferation may compensate for continuous activation and death of naive CD4⁺ T cells but may also have negative consequences for protective immunity. Here we show that naive CD4⁺ T cells that have proliferated in the periphery are characterized by a highly restricted oligoclonal TCR repertoire. Additionally these cells, which constitute the majority of naive CD4⁺ T cells in the elderly, display signatures of recent TCR engagement. Our results demonstrate for the first time that peripheral post‐thymic proliferation of naive CD4⁺ T cells in healthy human individuals causes a significant contraction of the peripheral TCR repertoire. This age‐dependent deterioration of CD4⁺ T cell immunity could entail ageing‐associated autoimmunity, increased susceptibility to infection or cancer and decreased efficiency of vaccination.