The immunological synapse is central to initiate an immune response, achieved by interaction between the antigen presented by CD1d and its cognate T cell receptor expressed on T lymphocytes. The unconventional T cells termed as NKT cells that are CD1d-confined, responding to lipid antigens are majorly grouped into type I and type II in literature so far. Their division is based on the gene composition of surface expressed αβ TCR and choice of antigen selection. Though cross reactivity between mouse and human NKT cells has been widely agreed, other species specific subsets exhibiting differential antigen specificity are yet to be explored. Currently as α-Galactosylceramide is being used as a potent immunotherapeutic agent in activating NKT cells, it is essential to understand the entire NKT cell repertoire to achieve an effective immune response. Here we present, a subset of human Vα24^-Jα18^-Vβ11^- NKT cells that bound the marker antigen of type I cells, α-Galactosylceramide and not α-Glucosylceramide in contrast to mouse Vα14^-Jα18^-Vβ8.1⁺ cells that showed preference to α-Glucosylceramide. It is interesting to note, their dual nature of binding to a range of α-linked and β-linked self-lipids. Surprisingly, crystal structures of such TCR/CD1d-α-Galcer complexes revealed a different docking topology involving an interaction with 6’OH position of the glycolipid that has never been observed with canonical type I TCR complexes solved to date. On the other hand, we have also determined crystal structures of type I NKT TCRs complexed with CD1d presenting β-linked ligands demonstrating a conserved docking orientation emphasizing the evolutionary selection of residues both on TCR and CD1d. Thus examining diverse repertoires of NKT cells would enhance our existing knowledge on understanding their antigen specificity and functional outcome.