Listeria monocytogenes(Lm) is a Gram-positive facultative intracellular pathogen that leads a biphasic lifecycle, transitioning its metabolism and selectively inducing virulence genes when it encounters mammalian hosts. Virulence gene expression is controlled by the master virulence regulator PrfA, which is allosterically activated by host- and bacterially-derived glutathione (GSH). The amino acid L-cysteine is the rate-limiting substrate for GSH synthesis in bacteria and is essential for bacterial growth. Unlike many bacteria,Lmis auxotrophic for L-cysteine and must import exogenous cysteine for growth and virulence. GSH is enriched in the host cytoplasm, and previous work suggests thatLmutilizes exogenous GSH for PrfA activation. Despite these observations, the import mechanism(s) for GSH remains elusive. Analysis of known GSH importers predicted a homologous importer inLmcomprised of the Ctp ABC transporter and the OppDF ATPases of the Opp oligopeptide importer. Here, we demonstrated that the Ctp complex is a high-affinity GSH/GSSG importer that is required forLmgrowth at physiologically relevant concentrations. Further, we demonstrated that OppDF are required for GSH/GSSG import in an Opp-independent manner. These data support a model where Ctp and OppDF form a unique complex for GSH/GSSG import that supports growth and pathogenesis. Additionally, we show thatLmutilizes the inorganic sulfur sources thiosulfate and H2S for growth in a CysK-dependent manner in the absence of other L-cysteine sources. These findings suggest a pathoadaptive role for partial cysteine auxotrophy inLm, where locally high GSH/GSSG or inorganic sulfur concentrations may signal arrival to distinct host niches.