To understand the early acute response to bacterial pathogens in lung tissue we investigated infection with the opportunistic pathogen Legionella pneumophila, the major cause of Legionnaire’s disease. It appears that memory T cells play a surprisingly important role in the innate response and are required for production of robust IFNγ production in the first few days after infection. The memory T cells rapidly infiltrate tissue after infection and are driven to produce cytokines independently of antigenic stimulation. Instead, IFNγ production by T cells is stimulated by cytokines produced by inflammatory dendritic cells. This work highlights a previously unappreciated pathway whereby inflammatory DC drive memory T cells to play a dominant role in the tissue restricted innate immune response to a pulmonary bacterial pathogen.