The RNA-binding protein CsrA is a global post-transcriptional regulator and controls many physiological processes and virulence traits. Deletion of csrA caused loss of virulence, reduced motility and production of xanthan gum, substantial increase in glycogen accumulation as well as enhanced bacterial aggregation and cell adhesion in Xanthomonas. How CsrA controls these traits is poorly understood. In this study, an iTRAQ-based proteomic analysis was conducted to compare the protein profile of wild-type strain X. citri subsp. citri (Xcc) and isogenic ∆csrA strain. Totally, 2374 proteins were identified, and 284 were considered to be differentially expressed proteins (DEP¬S), among which 151 proteins were up-regulated and 133 were down-regulated in ∆csrA strain with respect to wild-type strain. Enrichment analysis and protein-protein interaction (PPI) network analysis showed that CsrA regulates bacterial secretion systems, flagella, and xanthan gum biosynthesis. Several proteins encoded by the gumB operon were down-regulated whereas proteins associated with flagellum assembly and type IV secretion system (T4SS) were up-regulated in the ∆csrA strain relative to Xcc306. These results were confirmed by GUS assay or western blot. RNA secondary structure prediction and gel shift assay indicated that CsrA binds to the Shine-Dalgarno (SD) sequence of virB5. In addition, the iTRAQ analysis identified 248 DEPs that were not previously identified in transcriptome analyses. Among them, CsrA regulates levels of 8 regulatory proteins (ColR, GacA, GlpR, KdgR, MoxR, PilH, RecX, and YgiX), 7 TonB-dependent receptors, and 2 ferric enterobactin receptors. Taken together, this study greatly expands understanding of the regulatory network of CsrA in Xcc.