Targeted protein degradation is a valuable strategy to eliminate disease-relevant proteins. Among other classes, proteolysis targeting chimeras (PROTACs) are bifunctional molecules that induce the proximity of a recruiter E3 ligase and the target protein of interest for ubiquitination and subsequent degradation by the proteasome. While most PROTACs are non-covalent interactors, covalent PROTACs may benefit from increased selectivity and altered pharmacodynamics, yet remain largely understudied. In this context, a gold-based metallo-PROTAC (AuPROTAC) was synthesized, consisting of a cyclometalated Au(III) complex based on a bidentate C^N-ligand, which induces covalent cysteine/selenocysteine-arylation in a gold-templated two-step mechanism. This was then linked to a cereblon binding moiety. The degradome of the covalent AuPROTAC was characterized by establishing a cycloheximide chase assay, which was performed in a non-proliferative steady-state cell culture system that maintained a static protein turnover and efficiently decouples protein degradation from down-regulation. The method was verified with the known SMARCA2 and PBRM1-degrader ACBI2. The AuPROTAC was found to degrade MERTK and TXNL1, while their degradation was successfully rescued by proteasome inhibition. Since MERTK does not contain a cysteine in the active binding pocket, AuPROTAC is believed to covalently modify this protein at an allosteric site, leading to its degradation by the proteasome. The PROTACs were found to affect protein half-lives in this cycloheximide chase assay. Therefore, proteome-wide degradation selectivity was further characterized by ranking degraded targets based on the acceleration of protein half-lives. Overall, the established approach can be used to efficiently explore degradomes of CRBN and VHL recruiter-based PROTACs.