Xyloglucans (XyGs) are the most abundant hemicellulose in the primary walls of land plants and is composed by highly decorated β(1→4) glucans. This polysaccharide constitutes a source of nutrients for many microorganisms, but its utilization by phytophatogenic bacteria of Xanthomonas genus is still poorly understood. In this study, we show that Xanthomonas citri subsp. citri uses xylogluco-oligosaccharides (XyGOs) as carbon source and we identify the molecular machinery employed by X. citri to depolymerize XyGs. The genes encoding XyGs-active enzymes were predicted from the X. citri genome, cloned in pET28a vector, expressed, purified and characterized, revealing specific roles in XyG deconstruction. To understand the X. citri response to this complex polysaccharide, we analyzed the transcriptome of X. citri grown in XyGOS compared to X. citri grown in glucose, revealing the differential expression of genes related to cell motility, inorganic ions transport and signal transduction mechanisms. Thus, besides to uncover novel enzymes with potential applications in biomass saccharification technologies, this work also shed light on a new role for XyGOs in modulating the metabolism of phytopathogens.