Prokaryotes create adaptive immune memories by acquiring foreign DNA snippets, known as spacers, into the CRISPR array1. In type II CRISPR-Cas systems, the RNA-guided effector Cas9 also assists the acquisition machinery by selecting spacers from the protospacer adjacent motif-flanked DNA2,3. Here we uncovered the first biological role of Cas9 that is independent of its dual RNA partners. Following depletion of CRISPR RNA (crRNA) and/or trans-activating CRISPR RNA, Neisseria apoCas9 stimulates spacer acquisition efficiency. Physiologically, Cas9 senses low concentrations of crRNA in cells with short CRISPR arrays, such as those undergoing array neogenesis or natural array contractions, and dynamically upregulates acquisition to quickly expand the small immune memory banks. As the CRISPR array expands, rising crRNA abundance in turn reduces apoCas9 availability, thereby dampening acquisition to mitigate autoimmunity risks associated with elevated acquisition. Although the nuclease lobe of apoCas9 alone suffices to stimulate acquisition, only full-length Cas9 responds to crRNA concentrations to boost acquisition in cells with low immunity depth. Finally, we showed that this activity is evolutionarily conserved across several type II-C Cas9 orthologues. Altogether, we established an auto-replenishing feedback mechanism in which apoCas9 safeguards CRISPR immunity depth by acting as both a crRNA sensor and a regulator of spacer acquisition.