The ash leaf-cone roller, Caloptilia fraxinella (Ely) (Lepidoptera: Gracillariidae) is an introduced leaf-mining moth of horticultural ash trees (Fraxinus Linnaeus; Oleaceae) in Western Canadian Prairie cities. Here, we identify the dominant parasitoid of this leaf-mining moth as Apanteles polychrosidis Vierek (Hymenoptera: Braconidae) and document its emergence pattern, courtship, mating, and host acceptance behaviours. Apanteles polychrosidis adult emergence is protandrous and mating occurs soon after female emergence. Male A. polychrosidis can mate multiple times in short sequence with a mean copulation time of 49 seconds. It is likely that A. polychrosidis overwinters in an alternate larval host, after emergence from C. fraxinella. Mated female A. polychrosidis readily parasitise an alternate host, the obliquebanded leafroller (Choristoneura rosaceana (Harris); Lepidoptera: Tortricidae), known to overwinter as larvae. Through rearing C. fraxinella pupae, we describe the remainder of the parasitoid complex of C. fraxinella, in order of parasitism rate, as Diadegma Förster (near Diadegmafenestrale (Holmgren)) (Hymenoptera: Ichneumonidae), three Sympiesis Förster species (Hymenoptera: Eulophidae) (Sympiesissericeicornis (Nees von Esenbeck), one near Sympiesisviridula (Thomson) and one unknown species), and Pteromalus phycidis (Ashmead) (Hymenoptera: Pteromalidae) and show that several Sympiesis species can be hyperparasitic on A. polychrosidis. Caloptilia fraxinella density within the tree canopy is highest in the lower canopy. Host density and abiotic factors such as temperature and light intensity do not influence the within-canopy distribution of most parasitoids except Sympiesis species, which preferred the northern canopy.