Regulating gene expression during infection is critical to the ability of pathogens to circumvent the immune response and cause disease. This is true for the group A Streptococcus (GAS), a pathogen that causes both invasive and non-invasive diseases. The control of virulence (CovR/S) two-component system has a major role in regulating GAS virulence factor expression, tailoring it in a disease-specific manner. We identified that the regulator of cov (RocA) protein functions through CovR/S to dramatically alter gene expression, including enhancing expression of more than a dozen immunomodulatory virulence factors. The regulatory activity of RocA reduces the virulence of GAS during invasive infection, as evident from Lancefield bactericidal assays and a murine bacteremia model of infection. While predicted to be a membrane-spanning kinase, we identified that only the membrane-spanning domains of RocA, not the dimerization or HATPase domains, are required for complementation of a rocA mutant strain. Thus, our data are consistent with RocA being a pseudokinase. How RocA functions through CovR/S remains to be fully elucidated, but we have determined that RocA enhances the ratio of phosphorylated to non-phosphorylated CovR. We propose a model in which RocA complexes with CovS and enhances CovS kinase activity. Consistent with this, Mg2+ and LL-37, which positively and negatively regulate CovS activity respectively, are attenuated in their activity in the absence of RocA. Thus, we propose that RocA, as a key accessory protein to the CovR/S system, influences the ability of GAS to modulate gene expression in response to host factors.