A defining feature of bacteria is the peptidoglycan cell wall that confers cell shape and protects cells from osmotic lysis. While peptidoglycan hydrolases, or autolysins, are required for incorporation of new cell wall material and for separation of daughter cells, dysregulated autolytic activity may have lethal consequences. The mechanisms controlling expression of these deadly enzymes remain to be fully understood. In a search for novel substrates of the ClpXP protease, we here identify a ClpXP controlled autolysin, CxcA, and show that it contributes to separation of Staphylococcus aureus daughter cells. We also show that CxcA contributes to conditional autolysis of ClpXP cells at sub-optimal growth temperatures. Additionally, we show that CxcA expression is positively controlled by a regulatory RNA, rbc1, transcribed from the antisense strand of cxcA. Strikingly, rbc1 is capable of in trans base pairing and recognize RNAs of other autolysins, such as Sle1, SsaA, EssH and SAUSA300_02503, whereby a conserved CHAP domain encoding sequence, serves as binding site for rbc1. We show that rbc1 allow S. aureus to strongly induce expression of CHAP-domain containing autolysins in response to decreasing temperature. We also show that Sle1 inactivation leads compensatory overexpression of CxcA, while CxcA inactivation leads to increased Sle1 expression during temperature changes. In this study, we demonstrate that the cell wall hydrolases CxcA and Sle1 of S. aureus are intricately regulated through various mechanism including ClpXP protease activity, RNA-RNA regulation, compensatory mechanisms and temperature sensory mechanisms.