Analyses of the available avian genomes revealed the presence of a second TCRδ locus in the Galliformes. This second TCRδ locus is nonsyntenic to the conventional TCRα/δ and is unusual in that the V genes are more related to IgH V genes (VH) than to TCR V genes. The second TCRδ is not found in another avian lineage, the passerine zebra finch. Rather the finch's conventional TCRα/δ locus contains VH genes that are expressed with the conventional Cδ gene, similar to what has been found in amphibians. A comparison between Galliformes and Passeriformes genomic organization suggests an origin of the second TCRδ in the former lineage involving gene duplication. Expression of these atypical TCRδ transcripts with a VH domain paired with Cδ was found in lymphoid tissues of both avian lineages. The configuration of the second TCRδ in chicken and turkey is reminiscent of the TCRδ duplication that is present in nonplacental mammals and provides insight into the origin of the uniquely mammalian TCRμ locus.