Recently, many immune-related genes have been extensively studied in ducks, but relatively little is known about their TCR genes. Here, we determined the germline and expressed repertoire of TCR genes in White Peking duck. The genomic organization of the duck TCRα/δ, TCRγ and unconventional TCRδ2 loci are highly conserved with their counterparts in mammals or chickens. By contrast, the duck TCRβ locus is organized in an unusual pattern, (Vβ)n-Dβ-(Jβ)2-Cβ1-(Jβ)4-Cβ2, which differs from the tandem-aligned clusters in mammals or the translocon organization in some teleosts. Excluding the first exon encoding the immunoglobulin domain, the subsequent exons of the two Cβ show significant diversity in nucleotide sequence and exon structure. Based on the nucleotide sequence identity, 49 Vα, 30 Vδ, 13 Vβ and 15 Vγ unique gene segments are classified into 3 Vα, 5 Vδ, 4 Vβ and 6 Vγ subgroups, respectively. Phylogenetic analyses revealed that most duck V subgroups, excluding Vβ1, Vγ5 and Vγ6, have closely related orthologues in chicken. The coding joints of all cDNA clones demonstrate conserved mechanisms that are used to increase junctional diversity. Collectively, these data provide insight into the evolution of TCRs in vertebrates and improve our understanding of the avian immune system.