Human Vδ2+ T cells form the predominant human γδ T cell population in peripheral blood and possess a semi-invariant Vγ9 and Vδ2 T cell receptor (TCR) chain pairing. This TCR repertoire allows Vδ2+ T cells to function in an innate-like manner towards pyrophosphate metabolites (PAg) and mount TCR-dependent immune responses to bacterial and parasitic pathogens. Here, we explored the heterogeneity of this Vδ2+ T cell immune response in human Plasmodium falciparum and cytomegalovirus (HCMV) infection. We find that subpopulations of Vδ2+ T cells express alternate and often expanded TCR clonotypes and often these expanded TCRs define a population of PAg unresponsive Granzyme (Gzm) K- CD16+ Vd2+ T cells (atypical Vd2+ T cells). Transcriptional profiling of Vγ9/Vδ2+ T cells indicated that clonally expanded atypical Vδ2+ T cells possess a natural killer cell-like transcriptome compared to PAg reactive GzmK+ Vγ9/Vδ2+ T cells. Using a controlled human malaria infection (CHMI) we found that an individual with a predominant clonally expanded atypical Vδ2+ T cell population fails to mount a response to in vivo P. falciparum infection in humans. Vδ2+ T cells are classically responsive to both PAg and inflammatory cytokines, we found that neither stimuli could induce the clonal selection of the Vδ2+ TCR. Moreover, four repeated CHMIs over two years in individuals with a predominant PAg reactive GzmK+ Vδ2+ T cell population failed to drive clonal selection. However, cytomegalovirus infection in individuals undergoing lung transplant or hematopoietic stem cell transplantation drove the emergence and selection of atypical Vδ2+ T cells. Together, we reveal an alternative compartment of human Vδ2+ T cells that are selected after acute viral infection and that may be an important avenue for harnessing these cells for anti-microbial immunotherapies.