Cytotoxic T lymphocytes play an important role in the elimination of virus-infected and tumour-transformed cells. CD8+ T cells rely on activation by dendritic cell (DC) and subsequent priming to exert appropriate effector functions. Both CD4+ T cell help and the provision of IL-2 have been linked to CD8+ T cell activation, but how these factors interact and what the role of DC in the process is remains unclear. Using a mouse model of HSV-1 infection, we have characterized early T cell activation and observed that HSV-specific CD8+ T cells increased CD25 expression as they accumulated in the lymph node draining the site of infection. The resulting heightened ability of CD8+ T cells to respond to IL-2 was crucial for their expansion, as demonstrated by the failure of CD25-deficient CD8+ T cells to accumulate in response to HSV infection. Interestingly, we found that this enhanced IL-2 responsiveness by HSV-specific CD8+ T cells not only required the presence of CD4+ T cells and CD40, but was also similarly impaired in mice lacking IL-15. Together with data showing that CD4+ T cells were directly responsible for rendering DC capable of providing IL-15 in vivo, these findings highlight the regulation of CD25 expression by virus-specific CD8+ T cells as a critical element through which DC integrate T cell help into effective CD8+ T cell priming.