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PrsA-like chaperones have been identified in a number of Gram-positive bacteria, where they are reported to function at the bacterial membrane-cell wall interface to assist in the folding of proteins translocated across the membrane; in some cases, these proteins have been found to be essential for bacterial viability. In this study, the contributions of PrsA2 and PrsA1 to<jats:italic>L. monocytogenes<\/jats:italic>growth and protein secretion were investigated<jats:italic>in vitro<\/jats:italic>and<jats:italic>in vivo<\/jats:italic>. Neither PrsA2 nor PrsA1 was found to be essential for<jats:italic>L. monocytogenes<\/jats:italic>growth in broth culture; however, optimal bacterial viability was found to be dependent upon PrsA2 for<jats:italic>L. monocytogenes<\/jats:italic>located within the cytosol of host cells. Proteomic analyses of<jats:italic>prsA2<\/jats:italic>mutant strains in the presence of a mutationally activated allele of the virulence regulator PrfA revealed a critical requirement for PrsA2 activity under conditions of PrfA activation, an event which normally takes place within the host cell cytosol. Despite a high degree of amino acid similarity, no detectable degree of functional overlap was observed between PrsA2 and PrsA1. 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