Dioxins are highly injurious environmental pollutants with proven toxicological effects on both animals and humans, but to date their effects on plants still need to be studied in detail. We identified a dioxin-inducible caleosin/peroxygenase isoform, PdPXG4, that is mostly expressed in leaves of date palm seedlings and exhibits a specific reductase activity towards the 13-hydroperoxide of C18:2 and C18:3 (HpODE and HpOTrE, respectively). After exposure to TCDD, lipid droplets (LDs) isolated from TCDD-exposed leaves were about 6.5-15.7-fold more active in metabolizing 13-HpOTrE compared with those isolated from non-exposed leaves. A characteristic spectrum of leaf dioxin-responsive oxylipins (LDROXYL) was detected in dioxin-exposed seedlings. Of particular importance, a group of these oxylipins, referred to as Class I, comprising six congeners of hydroxides fatty acids derived from C18:2 and C18:3, was exclusively found in leaves after exposure to TCDD. The TCDD-induced oxylipin pattern was confirmed in vitro using terbufos, a typical inhibitor towards the PdPXG4 peroxygenase activity. Of particular interest, the response of terbufos-pretreated protoplasts to TCDD was drastically reduced. Together, these findings suggest that PdPXG4 is implicated in the establishment of a dioxin-specific oxylipin signature in date palm leaves soon after their exposure to these pollutants.