Plant pathogenic bacteria exerts their pathogenicity through the injection of large repertoires of type III effectors (T3Es) into plant cells, a mechanism controlled in part by type III chaperones (T3Cs). In Ralstonia solanacearum, the causal agent of bacterial wilt, little is known about the control of type III secretion at the post-translational level. Here, we provide evidence that the HpaB and HpaD proteins do act as bona fide R. solanacearum class IB chaperones that associate with several T3Es. Both proteins can dimerize but do not interact with each other. After screening 38 T3Es for direct interactions, we highlighted specific and common interacting partners, thus revealing the first picture of the R. solanacearum T3C-T3E network. We demonstrated that the function of HpaB is conserved in two phytopathogenic bacteria, R. solanacearum and Xanthomonas campestris pv. vesicatoria (Xcv). HpaB from Xcv is able to functionally complement a R. solanacearum hpaB mutant for hypersensitive response elicitation on tobacco plants. Likewise, Xcv is able to translocate a heterologous T3E from R. solanacearum in an HpaB-dependent manner. This study underlines the central role of the HpaB class IB chaperone family and its potential contribution to the bacterial plasticity to acquire and deliver new virulence factors.