Norway spruce (Picea abies) is an economically and ecologically important tree species that grows across northern and central Europe. Treating Norway spruce with jasmonate has long-lasting beneficial effects on tree resistance to damaging pests, such as the European spruce bark beetle Ips typographus and its fungal associates. The potential involvement of (epi)genetic mechanisms in this long-lasting jasmonate-induced resistance (IR) has gained much recent interest, but remains largely unknown. In this study, we treated 2-year-old spruce seedlings with methyl jasmonate (MeJA) and challenged them with the I. typographus vectored necrotrophic fungus Grosmannia penicillata. MeJA treatment reduced the extent of necrotic lesions in the bark and thus elicited IR to the fungus. The transcriptional response of spruce bark to MeJA treatment was analyzed over a 4-week time course using mRNA-seq. This analysis provided evidence that MeJA treatment induced a transient upregulation of jasmonic acid, salicylic acid and ethylene biosynthesis and downstream signaling genes. Additionally, genes encoding components of the RNA-directed DNA methylation pathway showed long-term repression, suggesting a possible role of DNA demethylation in the maintenance of MeJA-IR. These results provide new clues about the potential mechanisms underpinning long-term MeJA-IR in Norway spruce.