Peptide/MHC complexes recognized by alloreactive T lymphocytes (TLs) have been identified, but their contribution to in vivo allo‐rejection is not known. We previously characterized the peptide pBM1, highly represented among endogenous H‐2K^b (K^b)‐associated peptides and critically required to induce full activation of H‐2^k monoclonal CD8⁺ TLs expressing the cognate TCR‐BM3.3. Here, we asked whether a pBM1/K^b‐specific TL subset could be detected within a polyclonal TL population rejecting allogeneic cells in vivo. We show that the proportion of pBM1/K^b‐binding CD8⁺ TLs increased from <0.04% in naïve mice to 3% of activated CD44⁺ CD8⁺ TLs in H‐2^k mice rejecting K^b‐expressing cells. Among these, TCR‐Vβ2 usage was greatly enriched, and 75% of them shared a TCR‐Vβ2 CDR3β motif with the prototype TCR‐BM3.3. Fewer than 5% of K^b‐reactive CD44⁺ CD8⁺ TLs not binding pBM1/K^b displayed this CDR3β motif. We found that the recurrent CDR3β motif of pBM1/K^b‐binding TLs was assembled from distinct V/D/J recombination events, suggesting that it is recruited upon immunization for its optimal TCR‐peptide/MHC fit. Thus, a CDR3β motif generated by a process akin to “convergent recombination” accounts for a sizable fraction of the alloreactive anti‐K^b TCR repertoire.