Clostridium difficile is a Gram-positive, spore-forming pathogen that is a leading cause of nosocomial diarrhea worldwide. Infection by C. difficile requires that its hardy, resistant spores germinate into vegetative cells as they transit through the gastrointestinal tract. Despite the critical importance of germination to C. difficile pathogenesis, little is known about the mechanisms that regulate this complex developmental process. Germination depends upon the enzymatic removal of the cortex, a protective layer of peptidoglycan that maintains spores in a dormant state. While cortex degradation is known to depend on the SleC cortex hydrolase being proteolytically activated by Csp family proteases in the Clostridia, how Csps sense and transduce the germinant signal to activate SleC remains unknown. In C. difficile,CspC was recently identified as a novel germinant receptor that directly senses bile salt germinants. Using genetic analyses, we demonstrate thatboth CspC and the CspBA fusion protease are essential for SleC activation during C. difficile germination. Mutational analyses indicate that the CspA domain of CspBA functions to stabilize CspC. Intriguingly, both CspA and CspC carry degenerate active sites, suggesting that two pseudoproteases coordinately regulate CspB protease activation during germination. Using biochemical and genetic methods, we demonstrate that CspB undergoes autoprocessing similar to other subtilisin-like serine proteases. By solving the first structure of the Csp family of proteases at 1.5 Å, we identify key structural domains required for its function. The structure reveals that, in contrast with previously studied bacterial subtilisins, the CspB prodomain remains stably bound to the mature enzyme. Collectively, our study provides molecular insight into Csp function, which may inform the development of inhibitors that can reduce C. difficile disease transmission and recurrence.