Whole genome duplication (WGD) is a mechanism critical to evolutionary change and speciation across the plant tree of life. Both conspecific genome doubling (autopolyploidy) and WGD following hybridization (allopolyploidy) may result in morphologically distinct lineages and hence may contribute significantly to species diversity. However, accurate phylogenetic reconstruction of allopolyploids and their component genomes remains a major challenge. The moss Physcomitrium pyriforme is a widespread species complex found across North America and Europe that exhibits subtle, continuous morphological variation evident in the recognition of 29 synonyms. We hypothesize that this species complex comprises numerous cytotypes resulting from repeated WGD events. We sampled over 300 populations of P. pyriforme across its North American and use a target capture approach to sequence 648 genes to construct a phylogenetic tree establishing relationships among P. pyriforme populations. We find multiple well-supported clades of haploid populations within P. pyriforme, potentially representing distinct species. Target capture data was additionally used to identify allopolyploid populations by assessing heterozygosity across genes, suggesting at least 60 allopolyploid populations across Eastern North America. Here we utilize the significant genetic resources generated by target capture sequencing, as well as a new approaches to subgenome allele phasing, to reconstruct the evolutionary history of lineages within P. pyriforme as well as the reticulate evolutionary history of allopolyploid lineages by identifying hybrid progenitors. WGD plays a substantial role in the evolution of the P. pyriforme complex and provides evidence for morphologically cryptic speciation via polyploidy.