Deep-branching phylogenetic relationships are often difficult to resolve because phylogenetic signals are obscured by the long history and complexity of evolutionary processes, such as ancient introgression/hybridization, polyploidization and incomplete lineage sorting. Phylogenomics has been effective in providing information for resolving both deep- and shallow-scale relationships across all branches of the tree of life. Concatenated and coalescence trees based on the plastid genome, nuclear SNPs and multiple nuclear genes suggest events of incomplete lineage sorting and/or ancient introgression during the diversification of Oleaceae. Additionally, there was extreme heterogeneity in the plastid substitution rates across the tribes. Furthermore, our results supported that post-speciation introgression/hybridization, rather than ILS, is the main factor for phylogenetic discordance among the five tribes. The tribe Oleeae is especially prone to ancient hybridization and polyploidy, and its most likely parentages are the ancestral lineage of Jasmineae or its sister group, which is a “ghost lineage”, and Forsythieae. However, ILS and ancient introgression are mainly responsible for the phylogenetic discordance among the four subtribes of tribe Oleeae. This study showcases that using diverse phylogenomic methods can facilitate untangling long and complex evolutionary processes of ancient introgression, paleopolyploidization and ILS.