Control of intracellular pathogens relies on priming of cytotoxic CD8+ T cells by dendritic cells (DC), but how precisely DC are activated in the process and how they instruct CD8+ T cells to differentiate into effector cells remains unclear. We demonstrate that virus-specific CD8+ T cell priming depended on the sequential stimulation of CD8+ DC by type I IFN and CD4+ T cells, where type I IFN ‘conditioned’ DCs become receptive to CD40/CD40L-mediated CD4+ T cell help. This two-step activation endowed antigen presenting CD8+ DC with the capacity to transpresent IL-15 to naïve CD8+ T cells, without which these were unable to respond to IL-2 with high affinity and failed to undergo effector differentiation. These findings reveal a complex in vivo interplay between type I IFN and CD4+ T cells in DC activation and CD8+ T cell priming and indicate a role for CD4+ T cells as potent amplifiers of innate signals required for adaptive immune responses.