Abstract The TCR is consisted of four chains: α (TCRα), β (TCRβ), γ (TCRγ), and δ (TCRδ) that are present in all jawed vertebrates. Birds are very important in terms of evolutionary aspects of the adaptive immune system, in which it bridges the evolutionary gap between mammals and other vertebrates. To gain better understanding into the genomic organization and complexity of birds’ TCR loci, we applied cross-reference error-correction sequencing approach by using Illumina and single-molecule real-time sequencing technology to resequence genomic regions of chicken TCR loci based on 10 mapped bacterial artificial chromosome clones. We did de novo classification of V and J genes for all four chains of the TCR loci according to our sequencing results using the Immunogenetics nomenclature. In sum, we identified 85, 8, and 37 TCR V gene segments in the chicken TCRα/TCRδ, TCRβ, and TCRγ loci, respectively. The phylogenetic analysis showed the Vα 7 and Vα family 4 gene sequences shared greater sequence similarity with mammalian species, whereas the other Vα segment sequences are evolutionary closer with sequences from bony fishes. The organization of chicken TCRβ locus is more similar to fish TCRβ locus over mammalian species, as chicken TCRβ locus has a single translocon of its V–D–J–C and exhibits significantly fewer Vβ gene segments. In this study, we present a highly precise genomic map for chicken TCR loci and phylogenetic relationships of TCR variable gene segments against other animal species and verified the relative stability of the receptor structure during evolutional process.