ABSTRACT: Each αβT cell receptor (TCR) functions as a mechanosensor. The TCR is comprised of a clonotypic TCRαβ ligand-binding heterodimer and the noncovalently associated CD3 signaling subunits. When bound by ligand, an antigenic peptide arrayed by a major histocompatibility complex molecule (pMHC), the TCRαβ has a longer bond lifetime under piconewton-level loads. The atomistic mechanism of this "catch bond" behavior is unknown. Here, we perform molecular dynamics simulation of a TCRαβ-pMHC complex and its variants under physiologic loads to identify this mechanism and any attendant TCRαβ domain allostery. The TCRαβ-pMHC interface is dynamically maintained by contacts with a spectrum of occupancies, introducing a level of control via relative motion between Vα and Vβ variable domains containing the pMHC-binding complementarity-determining region (CDR) loops. Without adequate load, the interfacial contacts are unstable, whereas applying sufficient load suppresses Vα-Vβ motion, stabilizing the interface. A second level of control is exerted by Cα and Cβ constant domains, especially Cβ and its protruding FG-loop, that create mismatching interfaces among the four TCRαβ domains and with a pMHC ligand. Applied load enhances fit through deformation of the TCRαβ molecule. Thus, the catch bond involves the entire TCRαβ conformation, interdomain motion, and interfacial contact dynamics, collectively. This multilayered architecture of the machinery fosters fine-tuning of cellular response to load and pMHC recognition. Since the germline-derived TCRαβ ectodomain is structurally conserved, the proposed mechanism can be universally adopted to operate under load during immune surveillance by diverse αβTCRs constituting the T cell repertoire.