Standard models of speciation assume strictly dichotomous genealogies in which a species, the ancestor, is replaced by two offspring species. The reality is more complex: plant species can evolve from other species via isolation when genetic drift exceeds gene flow; lineage mixing can give rise to new species (hybrid taxa such as nothospecies and allopolyploids). The multi–copy, potentially multi–locus 5S rDNA is one of few gene regions conserving signal from dichotomous and reticulate evolutionary processes down to the level of intra-genomic recombination. Here, we provide the first high-throughput sequencing (HTS) 5S intergenic spacer (5S – IGS) data for a lineage of wind-pollinated subtropical to temperate trees, the Fagus crenata – F. sylvatica s.l. lineage, and its distant relative F. japonica. The observed 4,963 unique 5S – IGS variants reflect a long history of repeated incomplete lineage sorting and lineage mixing since the early Cenozoic of two or more paralogous-homoeologous 5S rDNA lineages. Extant species of Fagus are genetic mosaics and, at least to some part, of hybrid origin.