The search for natural product-based biopesticides from endophytic fungi is an effective tool to find new solutions. In this study, we studied a pre-selected fungal endophyte, isolate YCC4, from the paleoendemism Persea indica, along with compounds present in the extract and the identification of the insect antifeedant and nematicidal ones. The endophyte YCC4 was identified as Phyllosticta capitalensis by molecular analysis. The insect antifeedant activity was tested by choice bioassays against Spodoptera littoralis, Myzus persicae and Rhopalosiphum padi and the in vitro and in vivo mortality was tested against the root-knot nematode Meloiydogyne javanica. Since the extract resulted an effective insect antifeedant, a strong nematicidal and lacked phytotoxicity on tomato plants, a comprehensive phytochemical study was carried out. The chemical study resulted in the identification of two new metabolites, metguignardic acid (4) and (-)-epi-guignardone I (14), along the known dioxolanones guignardic acid (1), ethyl guignardate (3), guignardianones A (5), C (2), D (7) and E (6), phenguignardic acid methyl ester (8), and the meroterpenes guignardone A (9) and B (10) and guignarenone C (12), (-)-guignardone I (13) and the phyllomeroterpenoid B (15). Among these compounds, 1 and 4 were effective antifeedants against both insect species, while 2 was only active on the aphid M. persicae. The nematicidal compounds were 4, 7 and 8. This is the first report on the insect antifeedant or nematicidal effects of these dioxolanone-type compounds. Since the insect antifeedant and nematicidal activity of the P. capitalensis extract depends on the presence of dioxolanone components, future fermentation optimizations are needed to promote the biosynthesis of these compounds instead of the meroterpenes.