CD4⁺ CD45RO⁺ T cells could mature freshly isolated human plasmacytoid dendritic cells (PDC) in a superantigen‐driven culture in a similar way to recombinant interleukin‐3 (IL‐3). Mature PDC expressed significantly higher levels of inducible costimulator ligand (ICOS‐L), but similar levels of CD80 and CD86, when compared to mature monocyte‐derived DC (moDC). We therefore directly compared the capacities of mature PDC and moDC to activate T cells. A similar T helper type 1 (Th1)/Th2 pattern of cytokines was generated in both systems, but significantly higher levels of IL‐3, IL‐4 and IL‐10 were induced by PDC. In T cells interacting with PDC, the ICOS/ICOS‐L costimulatory pathway played a pre‐eminent role in the generation of IL‐3 and IL‐10, CD28 was central to the induction of IL‐2, and both pathways were equally important for the generation of other cytokines. In cocultures with moDC, the CD28 pathway was dominant over ICOS under all circumstances, except for the ICOS‐mediated release of IL‐10. In general, our data demonstrate an eminent role of ICOS in the interaction of T cells with PDC, and thus modify the current paradigm of CD28 dominance for the costimulation of T cells interacting with professional antigen‐presenting cells. In particular, our data highlight the role of ICOS in the generation of IL‐3, a factor central to the biology of human PDC.