Annonaceae is a major tropical plant family particularly diverse in tropical rain forests of the world. Although the classification and systematics of the family has significantly improved over the past decade, the most recent classification was based on a reduced set of plastid markers and incomplete genus‐level taxon sampling. This classification recognised 4 subfamilies and 20 tribes. Yet, several important problems persisted, especially the phylogenetic placement of the African genus Meiocarpidium, resolution of intertribal relationships within subfamily Malmeoideae, resolution and classification within the diverse tribe Miliuseae with 23 genera, and the contrasting placement of the liana genus Artabotrys when using nuclear versus plastid data. Here, using a previously published Annonaceae‐specific nuclear bait kit, we generated for the first time a complete genus‐level (108 taxa) phylogenomic tree of the family based on 373 loci. We show that Meiocarpidium is sister to Ambavioideae and should be considered as a tribe and not a separate subfamily. Artabotrys is recovered as belonging to tribe Duguetieae, and not Xylopieae as previously inferred based on plastid data, and is sister to two other African liana genera, Letestudoxa and Pseudartabotrys. Finally, we were able to resolve intertribal relationships within subfamily Malmeoideae and most of the relationships within tribe Miliuseae. Nevertheless, we recovered strong gene conflict mainly at the backbone of the tribe, probably linked to a rapid diversification at its origin, leading to substantial incomplete lineage sorting. We suggest that this conflict will be hard to resolve. Using this novel phylogenomic framework we recognize 25 subtribes, 21 as new, to improve the infrafamilial classification of Annonaceae.