Summary The genus Riccia is the most speciose of the Marchantiopsida, the complex thalloid liverworts. In contrast to the predicted ancestral liverwort and the majority of extant liverworts that are dioicous, most Riccia species are monoicous. Both the gametophyte and the sporophyte generations have undergone regressive evolution in Riccia, with the sporophyte lacking many adaptations for spore dispersal. Phylogenetic reconstructions suggest multiple transitions between dioicy and monoicy, and vice versa, within the Riccia. We analysed the genomes of two Riccia species and the transcriptomes of two additional Riccia species to explore the evolution of sexual systems and investigate genomic signatures of regressive evolution. Genomic analyses suggest a transition from dioicy to monoicy at the base of the Riccia clade and a subsequent reversion to dioicy with the concomitant evolution of a new sex chromosome, followed by further transitions back to monoicy. Additionally, Riccia species exhibit significant losses of transcription factors known to control aspects of sporophyte and gametophyte development. Comparisons with the monotypic sister genus, Ricciocarpos, suggest independent evolutions to both monoicy and reductive morphologies in the two genera. The reductive morphology has facilitated their colonization of extreme habitats but has perhaps canalized them to remain there.