Haematopoietic stem cells primarily reside in the bone marrow where they proliferate and differentiate to continuously generate the effector cells that drive immune responses. However, in response to inflammation some haematopoietic stem and progenitor cells (HSPC) are recruited to peripheral tissue sites where they undergo a process termed extramedullary haematopoiesis. Contrasting this established paradigm, here we show residence and differentiation of HSPC in healthy gingiva, a key oral barrier, in the absence of overt inflammation. We initially determined that a novel population of monocytes in the gingiva could be locally maintained and subsequently identified not only monocyte progenitors, but diverse HSPC populations in the gingiva, which could give rise to multiple myeloid cell lineages. Unexpectedly, gingiva HSPC possessed similar differentiation potentials, reconstitution capabilities and cellular heterogeneity to bone marrow HSPC. However, the gingival HSPCs responded differently to external inflammatory insults, responding to oral but not systemic inflammation. Combined we highlight a novel pathway of myeloid cell development at a healthy barrier site and define a separate, gingiva-specific HSPC network supporting generation of a proportion of the innate immune cells that police this unique barrier site.