Ferns have notoriously immense genomes and very high chromosome numbers, hypothesized to be consequences of repeated rounds of whole-genome duplication (WGD). This genome complexity has hampered efforts to elucidate fundamental aspects of fern biology and land plant evolution through genome-enabled research. Here we delve into the genome assembly for the model fern species Ceratopteris richardii. This genome reveals a history of remarkably dynamic genome evolution including two WGDs over 300 million years of evolution in the fern lineage leading to Ceratopteris, and rapid changes in genome content and structure following the most recent WGD approximately 60 million years ago. These changes include massive gene loss, rampant tandem duplications, and multiple horizontal gene transfers from bacteria, contributing to the diversification of gene families in Ceratopteris. The insertion of transposable elements into introns has led the large size of the Ceratopteris genome and to exceptionally long genes relative to other plants. Gene family analyses indicate that genes directing seed development were co-opted from those controlling development of fern sporangia, providing insights into seed plant evolution.