DC often require stimulation from CD4+ T cells to propagate CD8+ T cell responses, but precisely how T cell help optimizes the priming capacity of DC and why this appears to differ between varying types of CD8+ T cell immunity remains unclear. We show that CD8+ T cell priming upon HSV-1 skin infection depended on DC receiving stimulation from both IFN-α/β and CD4+ T cells to provide IL-15. This was not an additive effect, but resulted from CD4+ T cells amplifying DC production of IL-15 in response to IFN-α/β. We also observed that increased innate stimulation reversed the helper-dependence of CD8+ T cell priming and that the innate stimulus, rather than the CD4+ T cells themselves, determined how ‘help’ was integrated into the priming response by DC. These findings identify T cell help as a flexible means to amplify varying suboptimal innate signals in DC.