Francisella tularensis, a gram-negative bacterium, is the etiological agent of the human disease, tularemia. Inhalation of as few as 10 bacteria can result in a rapidly progressing, disseminating, and often lethal infection. The biology and pathogenesis of Francisella within the lung following inhalation is not well understood. In vitro, the bacterium replicates within macrophages, but the cellular targets and intracellular niche within an animal host are unknown. We determined the suite of cells infected by Francisella during inhalation-acquired tularemia and assessed how pulmonary innate immune cell populations are impacted during infection. Initially, alveolar macrophages were the predominant host cell for replicating Francisella. Later, monocytes and neutrophils were recruited to the lung and neutrophils, normally potent microbial killers, became a major host cell for bacterial replication. Francisella was also found within interstitial macrophages, monocytes, dendritic cells, and alveolar type II epithelial (ATII) cells. Given the relative abundance of infected macrophages and monocytes during pulmonary disease, we assessed the importance of chemokine receptor, CX3CR1, which facilitates cell recruitment from the blood into infected tissues. Responding to Francisella infection, CX3CR1-deficient mice demonstrated increased monocyte and neutrophil recruitment into the lung over wild-type mice, though the infected cell profile and bacterial burden in lungs, liver, or spleen throughout the disease course were similar, indicating that this receptor did not play a critical role during pulmonary tularemia. Of all the identified infected cell types in the lung, only ATII cells are stationary structural cells. ATII cells possess many properties important to respiratory function including the production of pulmonary surfactant which maintains lung surface tension and contributes to protection against infectious agents. Francisella invaded ATII cells via host-cell dependent processes, and the bacterium replicated equally well within ATII cells as within macrophages. We isolated an insertion mutation disrupting the Francisella gene, ripA, that ablated the bacterium's ability to replicate within ATII cells but not macrophages. This strain was significantly attenuated in a mouse model of tularemia suggesting that infection of ATII cells is an important component of Francisella virulence and pathogenesis.