The type 3 secretion system (T3SS), also known as an injectosome, is a widespread macromolecular nanomachine that enables the delivery of bacterial effector proteins directly from bacterial cytosol into the cytosol of the host cells. Most T3SS subunits are genetically and structurally conserved among different Gram-negative bacteria, but there are some additional components that are distinct and species specific. In the genus Bordetella, these include the small T3SS protein subunits BscX and BscY, homologous to the Yersinia YscX and YscY proteins. These proteins appear to be a part of the export gate, orchestrating the secretion of early substrates, but their structure and function in the Bordetella T3SS apparatus remain unknown. Using nuclear magnetic resonance (NMR) spectroscopy, we determined the solution structure of the heterodimeric complex of BscX and BscY proteins, revealing that the six helical fold of BscY is wrapped by BscX made up by the N-terminal unstructured region and three C-terminal helices. Individual DbscX or DbscY deletion mutants of B. bronchiseptica did not exert any cytotoxic activity towards HeLa cells, indicating that presence of the BscX-BscY heterodimer is critical for proper function of the secretion apparatus. Moreover, removal of the first 22 amino acids from BscX rendered the bacterial mutant non-cytotoxic on HeLa cells, indicating that the N-terminal unstructured region of BscX is functionally important. In summary, the BscX and BscY proteins are required for function of the T3SS apparatus and delivery of the BteA effector of B. bronchiseptica into host cells.