Skin is a barrier tissue that is exposed to the environment and therefore susceptible to infection. During skin infection with herpes simplex virus-1, T cells infiltrate skin and are crucial for protection. Following resolution, memory T cells that are able to rapidly respond to secondary infection are generated. Resident memory T cells (TRM) remain at sites of previous infection in barrier tissues. These cells do not recirculate and provide superior protection against reinfection compared to circulating memory T cells. Resident CD8+ T cells have been described in the epithelial layer of several barrier organs following infection, whereas CD4+ memory T cells have been found to be sub-epithelial and to recirculate between blood and peripheral tissues. Using T cell depleting antibodies that deplete T cells only when they are in the bloodstream, as well as parabiosis and Kaede transgenic mice, we demonstrate that memory CD4+ T cells in skin are comprised of two populations. One rapidly recirculates between blood and skin, and the other does not recirculate and persists long term at the site of infection. At steady-state these populations of CD4+ T cells are present in skin at low numbers, with recirculating cells making up the majority. However, at memory following infection, resident CD4+ T cells have increased and outnumber recirculating CD4+ cells. These resident CD4+ T cells can also be generated in skin by treatment with the non-specific irritant DNFB. Furthermore, we reveal that hair follicle-derived chemokines are involved in retaining resident CD4+ memory T cells in skin, and that the majority of CD4+ T cells that respond to secondary infection are located in hair follicles. This project reveals the existence of a population of non-recirculating CD4+ T cells that exist at high numbers following skin damage and provides a mechanism to explain how resident cells are retained in skin, thus expanding our knowledge on T cell responses that are crucial for protection at barrier sites.