Control of intracellular pathogens relies on priming of cytotoxic CD8+ T cells (CTL) by dendritic cells (DC). Although it is well established that this process often requires T cell help, precisely how CD4+ T cells aid in the process and how this enables DC to instruct naïve CTL to differentiate into effector cells remains unclear. We have addressed these questions in a Herpes simplex virus (HSV) skin infection model, where lymph node-resident CD8+ DC play a central role in stimulating virus-specific CTL. Our observations show that HSV-specific CTL priming not only required CD4+ T cells, but also depended on the in vivo stimulation of CD8+ DC via the IFN-α/β-receptor (IFNaR). Intriguingly, we found that these two signals (T cell help and IFN-α/β) synergized to induce IL-15 production by CD8+ DC, which in turn was necessary for CTL priming. Together with complementary results in another model of helper-dependent CTL priming, our findings demonstrate a previously unappreciated functional cooperation between T cell help and innate signals. Rather than CD4+ T cells delivering unique ‘licensing’ signals to DC or directly eliciting DC activation as suggested by current models of T cell help, we propose a new modelwherein T cell help enhances CTL responses by amplifying the strength of innate signals in DC.