SUMMARY The response regulator CpdR couples phosphorylation events in Caulobacter crescentus with the AAA+ protease ClpXP to provide punctuated degradation of crucial substrates involved in cell cycle regulation. CpdR functions like an adaptor to alter substrate choice by ClpXP, however it remains unclear how CpdR influences its multiple targets. Here we show that, unlike canonical ClpXP adaptors, CpdR alone does not strongly bind its substrate. Instead, CpdR binds the N-terminal domain of ClpX and prepares (primes) the unfoldase for substrate engagement. This priming creates a recruitment interface that docks multiple substrates and additional adaptor components. We show that adaptor dependent priming of ClpX avoids concentration-dependent inhibition that limits traditional, scaffolding adaptors. Phosphosignaling disrupts the adaptor-protease interaction and mutations in CpdR that impact ClpX binding tune adaptor activity and biological function. Together, these results reveal how a single adaptor can command global changes in proteome composition through priming of a protease.