Repeat exposures to Plasmodium falciparum (Pf) does not rapidly induce the development of long-lived malaria immunity, and antibody responses induced by vaccines have short-lived protection. Vδ2 T cells are a subset of γδ T cells that act to enhance the inflammatory immune response to malaria. In addition to innate responsiveness, we propose that Vδ2 T cells contribute directly to malarial antibody development. We investigated the role of humanVδ2 T cells in antigen-presentation and B cell activation by utilising experimental and naturally-acquired malaria infection models. We co-cultured malaria-naive healthy peripheral blood mononuclear cells with blood-stage Pf, and observed increased Vδ2 T cell expression of both antigen-presenting cell (APC) surface antigens, HLA-DR, CD86 and CD40, and B cell activating surface antigens, CD40L and ICOS. In parasite co-cultures, malaria-naive Vδ2 T cells produced pro-inflammatory cytokines, IFNγ and TNF, but not cytokines previously implicated in malaria antibody induction, IL-4, IL-10 or IL-21. However, Vδ2 T cells from individuals with an acute, naturally-acquired malaria infection did produce antibody-inducing cytokines IL-10 and IL-21. We confirmed this phenotype in an Induced Blood-stage Malaria trial (IBSM), where we intravenously inoculated malaria-naive adults (n = 12) with blood-stage Pf. In this cohort, we observed increased Vδ2 T cell expression of surface antigens HLA-DR, CD86 and ICOS, at fifteen days post-inoculation. Data shows the induction of an APC/B cell activating Vδ2 T cell phenotype after malaria-naive Pf infection both in vitro and during an experimental IBSM model. Furthermore, we show the relevance of this phenotype in natural-acquired malaria, demonstrated by increased production of cytokines related to B cell activation during active infection. These results identify a novel and unconventional Vδ2 T cell phenotype activated during Pf infection.