Successful viral infection of the host involves navigating complex trans-kingdom interactions between the virus, host immune response and resident microbiome. Varicella Zoster Virus (VZV) primary infection manifests as disseminated skin disrupting vesicular lesions, which permits the translocation of resident riboflavin synthesising microbes. Critically, resident T cell populations such as Mucosal Associated Invariant T (MAIT) cells can rapidly respond to riboflavin-producing microbes with robust interferon (IFN)-γ, tumour necrosis factor (TNF) and granzyme B production, thereby also creating an environment likely to impair efficient viral replication. We showed that VZV downregulates expression of the MAIT cell cognate antigen presenting molecule MR1, potentially mitigating any downstream impacts of MAIT cell-microbiome engagement (Purohit et al., JID, 2021). Further, we recently demonstrated that VZV can directly infect MAIT cells (Purohit et al., Front Immunol, 2023). In the current study, we examined the impact of VZV infection on the functional capacity of MAIT cells. Using flow cytometry, we interrogated activation levels, cytokine response, cytolytic capacity of both VZV infected (VZV antigen positive) and VZV exposed (VZV antigen negative) MAIT cells to TCR dependent (5-OP-RU), cytokine driven (interleukin (IL)-12/IL-18) and combination (5-OP-RU + IL-12/IL-18) stimuli. We demonstrate that both VZV exposed and infected MAIT cells exhibit significantly lower activation levels and abrogated cytokine expression in response to TCR dependent, independent and combined stimulation. Furthermore, we reveal compromised cytolytic capacity of both VZV exposed and VZV infected MAIT cells in response to monocytes treated with intact riboflavin synthesising bacteria. Using live microscopy, we also find that VZV impairs the wound healing functionality of MAIT cells in vitro. These findings reveal a multifaceted immune-evasive strategy employed by VZV to counteract MAIT cell functionality.