Control of intracellular pathogens relies on priming of cytotoxic CD8⁺ T cells (CTL) by dendritic cells (DC). However, how DC are activated, 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) and toll-like receptor 3 (TLR3). While only the IFN-α/β signal was crucial for the MHCII and CD40 upregulation of CD8⁺ DC in response to the skin infection, IFNaR and TLR3 were critical for driving IL-15 and IFN-l secretion by CD8⁺ DC. This pattern of cytokine secretion was in turn found to be essential for optimal HSV-specific CTL responses. Intriguingly, stimulation of IFNaR and TLR3 only yielded IL-15 and IFN-l levels sufficiently high to support CTL priming if the CD8⁺ DC also received ‘help’ from CD4⁺ T cells. These results demonstrate a previously unappreciated functional cooperation between CD4⁺ T cells and innate signals. Thus, rather than CD4⁺ T cells delivering unique ‘licensing’ signals to DC or directly eliciting DC activation when innate signals fail to achieve this as suggested by current models of T cell help, we propose that CD4⁺ T cells ‘help’ CTL responses by modulating the strength with which DC respond to innate signals.