Cultivated wheats derive from an intricate history of three genomes, A, B and D, present in both diploid and polyploid species. It was recently proposed that the D genome originated from an ancient hybridization between the A and B lineages. However, this result has been questioned and a robust phylogeny of wheat relatives is still lacking. Using transcriptome data from all diploid species and a new methodological approach, our comprehensive phylogenomic analysis revealed that more than half of the species descend from an ancient hybridization event, but with a more complex scenario involving a different parent than previously thought: Aegilops mutica, an overlooked wild species, instead of the B genome. We also detected other extensive gene flow events that could explain long-standing controversies in the classification of wheat relatives.