Coxiella burnetii is a Gram-negative intracellular pathogen that causes Q fever, a debilitating disease in both animals and humans. Macrophage infectivity potentiator (Mip) proteins catalyze the folding of proline-containing proteins through their peptidyl prolyl cis-trans isomerase (PPIase) activity. Mip has been shown to play an important role in the virulence of several pathogenic bacteria but to date its role in pathogenesis has not been investigated in C. burnetii. Attempts to mutate the Mip homologue in C. burnetii, Cbmip (CBU0630), proved unsuccessful. Therefore to study the functional role of CbMip, small pipecolic acid based compounds that have been reported to inhibit the activity of Mip proteins from other bacteria were investigated. Using a protease coupled PPIase assay the small pipecolic acid based compounds were demonstrated to be potent inhibitors of CbMip PPIase enzyme activity. These CbMip inhibitors were found to significantly reduce the intracellular replication of C. burnetii Phase II Nine Mile Strain RSA439 (NMII) in both HeLa and THP-1 cells over 5 days as determined by qPCR and by intracellular staining of infected cells. The CbMip inhibitors were also found to inhibit the growth of NMII strains in axenic culture and comparative proteomic analysis of C. burnetii cultures revealed that over 200 proteins were significantly affected upon exposure to CbMip inhibitors. Furthermore, CbMip inhibitors demonstrated protective activity in vivo and significantly improved the survival of Galleria mellonella larvae infected with C. burnetii NMII. Since C. burnetii NMII lacks the full length lipopolysaccharide which is essential for virulence in vivo, the activity of these small molecule CbMip inhibitors was also assessed against the virulent C. burnetii Phase I Nine Mile Strain RSA439 (NMI) and were found to effectively inhibit the growth of C. burnetii NMI in axenic media. Our data shows that CbMip may be essential for C. burnetii replication and that inhibition of CbMip may represent a novel target for antimicrobial therapies against C. burnetii.