Pneumonia is the primary infectious cause of mortality for young children and the emergence of antibiotic resistance has decreased the efficacy of available therapeutics. Mucosal-associated invariant T (MAIT) cells respond to pathogens that cause pneumonia by recognizing microbial derivatives of riboflavin (vitamin B2) synthesis presented by the MHC class I-related (MR1) molecule. However, the cells that present these microbial metabolites remain unknown. Here, we demonstrate that type-17 MAIT cells respond to diverse isolates of the extracellular bacterial pathogen Acinetobacter baumannii and are the primary IL-17A producers during pulmonary infection, promoting bacterial clearance. Both hematopoietic and non-hematopoietic cells mediate MR1 presentation within the lungs and mediastinal lymph nodes (meLNs), with an Mr1f/f conditional knockout indicating redundancy among antigen-presenting cells (APCs). Conversely, the type-1 MAIT cell response to the intracellular bacterial pathogen Francisella tularensis requires MR1 presentation by type-2 conventional dendritic cells (cDC2s) within meLNs and ablation of these cells or their expression of MR1 renders animals more susceptible to the infection. A novel Mr1FLAG reporter indicated that A. baumannii enhanced MR1 protein expression by macrophages and pulmonary fibroblasts, while F. tularensis increased expression by cDC2s. These results demonstrate that microbial tropism dictates which APCs mediate MR1 presentation of metabolites and identify novel therapeutic targets for bacterial pathogens that cause pneumonia.