Cultivated hexaploid oat has three different sets of nuclear genomes (A, C, D), but its evolutionary history remains elusive. A multiplexed shotgun sequencing procedure was explored to acquire maternal phylogenetic signals from chloroplast and mitochondria genomes of 25 Avena species. Phylogenetic analyses of the acquired organelle SNP data revealed a new maternal pathway towards hexaploids of oat genome evolution involving three diploid species (A. ventricosa, A. canariensis and A. longiglumis) and two tetraploid species (A. insularis and A. agadiriana). Cultivated hexaploid A. sativa acquired its maternal genome from an AC genome tetraploid close to A. insularis. Both AC genome A. insularis and AB genome A. agadiriana obtained a maternal genome from an ancient A, not C, genome diploid close to A. longiglumis. Divergence dating showed the major divergences of C genome species 19.9-21.2 million years ago (Mya), of the oldest A genome A. canariensis 13-15 Mya, and of the clade with hexaploids 8.5-9.5 Mya. These findings not only advance our knowledge on oat genome evolution, but also have implications for oat germplasm conservation and utilization in breeding.