The T cell receptor (TCR) presents on the cell surface of T lymphocytes in a membrane-bound complex inclusive of CD3 co-receptors. ~230 million years ago, a duplication event of the CD3γ/δ gene resulted in distinct CD3γ and CD3δ genes. As we currently understand, all mammals possess separate CD3γ and CD3δ genes whilst other vertebrate species possess a fusion CD3γ/δ gene. The species-specific divergences of TCR architecture and function must be understood for T-cell research within varying non-human immune systems. Here, we used cryo-electron microscopy to determine the structure of a chicken αβ TCR-CD3, at 3.06Å resolution. In terms of co-receptor placement with respect to each other, the arrangement of the complex is similar to that previously solved in human αβ and γδ TCR complexes. Strict conservation of transmembrane and CD3 membrane proximal charged interactions, between evolutionarily distinct species, indicate their imperative role in TCR formation and function. The chicken TCR possesses a mobile extracellular domain, adopting conformational heterogeneity within the antigen-binding domain. This is strictly opposed to the observed rigid human αβ TCR and more akin to the highly flexible human γδ TCR. This flexibility is likely caused by a lack of shape and charge complementarity between chicken TCR constant domains and the CD3 co-receptors as well as less biochemically ordered TCR connecting peptides. Our findings reveal the presentation of the αβ TCR extracellularly can differ broadly between species and clarify that the human αβ TCR may have distinctly evolved to be rigid in nature.