T cell receptor (TCR) recognition of peptide–major histocompatibility complexes (pMHC) is characterized by a highly conserved docking polarity. Whether the canonical TCR–pMHC polarity is driven by recognition or signaling constraints remains unclear. Using “reversed docking” TRBV17+ TCRs from the naïve mouse CD8+ T cell repertoire that recognize the H-2Db–NP366 epitope of Influenza A virus, we demonstrate that their inability to support T cell activation and in vivo recruitment is a direct consequence of reversed docking polarity and unrelated to TCR–pMHCI binding. The canonical TCR–pMHCI docking polarity optimally localizes CD8/Lck to the CD3 complex, which is prevented by reversed polarity TCR–pMHCI engagement. Thus, a canonical docking topology at the highly diverse TCR–pMHC interface is critical for an effective immune response.