T cell tolerance is established and maintained through various mechanisms, the critical component being the persistence of the specific Ag. However, at the molecular level, the nature of the recovering TCR repertoire following breakdown of tolerance is unknown. We address this important question by following κ light chain constant region (Cκ)-specific CD4+ T cells of κ light chain knock-out (κ−/−) mice born to κ+/− mothers. These cells, which were in contact with maternal κ+ Igs from early ontogeny until weaning, were strongly tolerized. Tolerance was reversible and waned with the disappearance of peptide Cκ 134–148 presentation in lymphoid organs, including the thymus. Whereas three specific Vβ-Jβ rearrangements emerged in the peptide Cκ 134–148-specific CD4+ T cell response of all regular κ−/− mice, soon after breakdown of tolerance only one of these rearrangements was detected. The two others displayed a significant delay in reappearance and were still rare at 26 wk of age, while the control proliferative response had already recovered 3 mo earlier. At 52 wk of age, a complete recovery of the three canonical Vβ-Jβ rearrangements was observed. Thus, although profoundly perturbed for several months, the T cell repertoire returns to equilibrium, highlighting the resilient nature of this system.