Antigen-presenting cells (APC), such as dendritic cells (DC) and macrophages, are critical for T-cell-mediated immunity. Although it is established that memory T cells accumulate and persist in peripheral tissues after the resolution of infection, whether this is also the case for APC remains unclear. Here, we report that CCR2-dependent cells infiltrate skin during acute infection with herpes simplex virus (HSV)-1 and subsequently give rise to localized populations of DCs and macrophages. These APC are found at elevated numbers at sites of resolved infection or inflammation compared with unaffected regions of skin. Importantly, this local accumulation of APC is sustained for prolonged periods of time and has important functional consequences, as it promotes interferon-γ responses by virus-specific CD4+ T cells upon localized challenge infection with HSV-1. Thus, our results highlight how infection history determines long-term changes in immune cell composition in skin and how different types of immune cells accumulate, persist and co-operate to provide optimal immunity at this critical barrier site.