Innate cellular immune responses are an important first line of defense against invading pathogens. Leukocyte migration from the bloodstream to a site of infection is mediated by chemotactic factors that are often host-derived. More recently, there has been a greater appreciation of the importance of bacterial factors driving chemoattraction and neutrophil behavior. The objectives of this work were to interrogate A. baumannii-dependent factors that determine neutrophil behavior in vivo. We developed the A. baumannii - zebrafish (Danio rerio) infection model. The transparency, genetic tractability and breadth of immune development of zebrafish make it an ideal model for studying mechanisms of host-pathogen interactions. We first demonstrated that neutrophils were the dominant phagocyte responder to A. baumannii infection, and that bacterial handling occurred within the phagolysosome. Isogenic bacterial mutants lacking expression of virulence effector proteins demonstrated that bacterial drivers of disease severity were conserved between zebrafish and mammals. We then explored bacterial-dependent factors driving neutrophil behavior in vivo and identified a thus far unknown mechanism that highlights a relationship between bacterial metabolism and host innate immune evasion.