Metals essential to biological systems are tightly regulated through various mechanisms to maintain cellular homeostasis. These metals play critical roles in modulating cell signaling and act as enzymatic cofactors for metalloproteins such as zinc finger (ZF) proteins. A hallmark of all zinc finger (ZF) proteins is their dependence on zinc for proper folding and function, coordinated through unique combinations of cysteine and/or histidine residues that serve as the basis for their classification. However, due to the nucleophilic nature of cysteine-thiol groups, ZFs are particularly susceptible to post-translational modifications (PTMs), resulting in structural and functional disruptions that lead to cellular dysfunction and contribute to various diseases. Interestingly, emerging evidence suggests that cysteine-rich ZFs are common targets of hydrogen sulfide (H₂S)-mediated persulfidation, a post-translational modification observed in eukaryotes. Despite advances in the field, many ZF proteins have yet to be thoroughly characterized biochemically, and the mechanisms underlying ZF persulfidation remain poorly understood. In our previous persulfide-selective proteomic studies, we identified two ZF proteins reactive with H2S, Rho-associated Coiled-Coil Kinase (ROCK1) and Poly-ADP-ribose polymerase 1 (PARP1). To explore the biochemical properties of ROCK1, we employed a reductionist approach using isolated zinc-binding domains within the cysteine-rich domain (CRD). Initial determinations of ROCK-CRD reveal its canonical metal coordination properties are analogous to LIM/PHD/RING-type ZFs. Further biochemical and structural analysis reveal that isolated ROCK-CRD mutants can coordinate metal with tight binding, utilizing a non-canonical ligand set in a manner typical of single-domain ZF proteins. To investigate the mechanism of ZF persulfidation, we isolated the DNA-binding ZF domains of PARP1. Here, our findings provide the first in vitro evidence of H₂S-mediated persulfidation of PARP1, supporting the hypothesis that this modification may be a conserved mechanism across all ZF types. Collectively, these studies deepen our understanding of ZF protein classifications and their regulation by gaseous signaling molecules and post-translational modifications, offering valuable insights for the development of targeted therapeutics.