Multiple genetic changes in the enteric pathogenYersinia pseudotuberculosishave driven the emergence ofYesinia pestis, the arthropod-borne, etiological agent of plague. These include developing the capacity for biofilm-dependent blockage of the flea foregut to enable transmission by flea bite. Previously, we showed that pseudogenization ofrcsA, encoding a component of the Rcs signalling pathway, is an important evolutionary step facilitatingY. pestisflea-borne transmission. Additionally,rcsD,another important gene in the Rcs system, harbours a frameshift mutation. Here, we demonstrated that thisrcsDmutation resulted in production of a small protein composing the C-terminal RcsD histidine-phosphotransferase domain (designated RcsD-Hpt) and full-length RcsD. Genetic analysis revealed that thercsDframeshift mutation followed the emergence ofrcsApseudogenization. It further altered the canonical Rcs phosphorylation signal cascade, fine-tuning biofilm production to be conducive with retention of thepgmlocus in modern lineages ofY. pestis. Taken together, our findings suggest that a frameshift mutation inrcsDis an important evolutionary step that fine-tuned biofilm production to ensure perpetuation of flea-mammal plague transmission cycles.