All complexes of T cell receptors (TCRs) bound to peptide–major histocompatibility complex (pMHC) molecules assume a stereotyped binding 'polarity', despite wide variations in TCR-pMHC docking angles. However, existing TCR-pMHC crystal structures have failed to show broadly conserved pairwise interaction motifs. Here we determined the crystal structures of two TCRs encoded by the variable β-chain 8.2 (V_β8.2), each bound to the MHC class II molecule I-A^u, and did energetic mapping of V_α and V_β contacts with I-A^u. Together with two previously solved structures of V_β8.2-containing TCR-MHC complexes, we found four TCR–I-A complexes with structurally superimposable interactions between the V_β loops and the I-A α-helix. This examination of a narrow 'slice' of the TCR-MHC repertoire demonstrates what is probably one of many germline-derived TCR-MHC interaction 'codons'.