Varicella zoster virus (VZV) is a ubiquitous virus within the human population. The ability of this virus to disseminate globally is due to the array of strategies it has evolved to evade multiple aspects of the host immune response. The live attenuated VZV vaccine has been reported to induce severe disseminated disease in those with CD1d and iNKT cell deficiencies, and people with such deficiencies also experience repeated viral reactivations and severe disease. Despite these observations, until now the interactions between VZV and the CD1d/iNKT cell axis has not been reported. Using surface and intracellular flow cytometry analysis on an immature T cell line we were able to identify the profound loss of CD1d at both the cell-surface and total protein level in both VZV-infected (viral antigen-positive) and VZV-exposed (viral antigen-negative) cells. Due to the loss of CD1d in VZV antigen-negative cells we used supernatant and transwell experiments to determine that the phenomenon was not due to a secreted factor and thus is likely to be dependent on contact with a VZV-infected cell. Quantitative PCR on the T cells incubated with VZV inoculum demonstrated a significant loss of CD1d transcript. In the context of peripheral blood mononuclear cell (PBMC) infection, CD1d was also downregulated on the cell-surface of VZV-infected primary B cells. Additionally, iNKT cells, as detected using a-GalCer loaded CD1d tetramer, were found to be permissive to VZV infection in PBMC samples, with ~20% of iNKT cells being VZV antigen-positive after 24 hrs. This study identifies VZV-mediated modulation of CD1d as a previously unrecognised immunomodulatory function of this virus that may enable evasion of iNKT cell responses during infection and provides evidence that VZV can directly infect iNKT cells.