Group A Streptococcus or Streptococcus pyogenes is a major human pathogen that causes a range of diseases, from minor skin and throat infections such as impetigo and pharyngitis, to severe invasive infections such as streptococcal toxic shock syndrome and necrotising fasciitis. GAS produces pili, hair-like protrusions from the bacterial cell surface that are involved in adhesion and colonisation of the host. These surface-exposed pili are immunogenic and therefore represent an attractive target for vaccine development. The pilus is encoded in the genomic region known as the fibronectin-collagen-T-antigen (FCT)-region, of which at least nine different types have been identified. The pilus operon encodes a backbone pilus protein (aka the T antigen), one or two accessory pilus proteins and a pilus assembly sortase enzyme. In this study we investigate expressing two of the most common FCT-types (FCT-3 and FCT-4) in the food-grade bacterium Lactococcus lactis for use as a mucosal vaccine. We show that mucosally delivered L. lactis expressing GAS pili generate specific antibody responses in rabbits. These antibodies were shown to have both a neutralising effect on bacterial adhesion, as well as facilitate immune-mediated killing of bacteria via opsonophagocytosis. Furthermore, intranasal immunisation of mice improved clearance rates of GAS after nasopharyngeal challenge. These results demonstrate the potential for a novel, pilus-based vaccine to protect against GAS infections.