Medicinal plants are conventionally used for wound healing, but their action mechanisms are still unknown. The present study evaluated the effect of topical administration of ointment containing dill (Anethum graveolens) essential oil (DEO) in the management of apoptosis and cell proliferation during MRSA-infected experimentally induced wound healing process in BALB/c mice model. The GC-FID and GC-MS techniques were used to analyze chemical composition of the essential oil. The mice were randomly divided into four treatment groups including negative control (sham), 2% and 4% DEO and mupirocin-treated animals. The full-thickness excisional wounds were inoculated by 5 × 10 colony-forming units of MRSA. In order to assess the effect of different concentrations of DEO on wounds infection, wound area, bacterial count, histopathological, immunohistochemical and RT-PCR analysis were evaluated. The GC-MS analysis identified α-phellandrene (47.3%), p-cymene (18.5%) and carvone (14.1%) as the main compounds of the essential oil tested here. Administration of DEO prevented bacterial growth and also reduced wound area in comparison to the control group. Topical administration of DEO significantly reduced the inflammatory phase and accelerated re-epithelialization, angiogenesis, fibroblast and collagen deposition. Moreover, the DEO-treated animals exhibited higher expressions of Bcl-2, p53 caspase-3, VEGF and FGF-2 in comparison to the control and mupirocin-treated groups (P < 0.05). Topical administration of DEO decreases the inflammatory phase by increasing p53 and caspases-3 expression. It triggers the proliferative phase by up-regulation of the Bcl-2, VEGF and FGF-2 expression and also up-regulates the collagen biosynthesis by enhancing the ERα expression level. Thus, ointment prepared from dill essential oil, in Iran, with its major compounds such as α-phellandrene, p-cymene and carvone can be used as an agent for accelerating the infected wound healing.