We pursued the concept that the TCR expressed by invariant NKT cells is functionally analogous to an innate immune receptor. As such, we considered the possibility that conserved regions of the heterodimer might control binding. Molecular modeling suggested that a hydrophobic patch, created upon TCR pairing, might have such a function. We find that that disruption of this patch by mutation of the TCRb chain ablated recognition of CD1d by the NKT TCR, but retained the capacity to functionally interact with MHCI and MHCII. Partial disruption of this region, however, did not detectably alter recognition of CD1d:aGal Cer or CD1d:OCH ligands. Unexpectedly, development of NKT cells expressing this partially disrupted TCR was substantially altered. In particular, PLZF was expressed at very low levels and the transcription factor Nfil3 (E4BP4) was induced. This expression pattern was similar to what is found in adipose resident NKT cells (arNKT cells). Indeed, we found that NKT cells bearing this mutant TCR selectively accumulated in the adipose tissue. Collectively, our data imply that developing NKT cells are directed into the arNKT cell lineage during thymic development as opposed to acquiring their distinct phenotype due to external cues in the adipose microenvironment.