Sporopollenin, the biopolymer that makes up the plant spore wall, is possibly one of the toughest biologically derived material known to man. The sporopollenin transfer hypothesis describes the process by which sporopollenin deposition shifted from the walls surrounding algal zygotes, to the walls surrounding post-meiotic spores in land plants. This was a key moment in land plant evolution, as this specialized cell wall imparted onto plants the ability to survive the harsh and desiccating environments of terrestrial life for extended periods of dormancy. To understand the mechanisms behind this heterochronic shift in sporopollenin deposition, we look at the function of a bHLH subclass II transcription factor in Marchantia polymorpha, MpbHLH37. By generating CRISPR/Cas-9 mediated knockout lines, our study shows MpbHLH37 to be a master regulator of secondary cell walls in spores, elaters, and the capsule wall of the M. polymorpha sporophyte. A finer look into the TEM ultrastructure of mutant sporophytes also discloses important homologies between the capsule wall of liverworts and the tapetum in tracheophytes and mosses. Finally, in a serendipitous turn of events, our study of heterozygous bhlh37 sporophytes sheds light on the epigenetic regulation of the diploid generation of M. polymorpha. This study extends our understanding of how sporopollenin production evolved from being directly regulated by the KNOX/BELL system in chlorophyte lineages, to being regulated by the bHLH subclass II genes downstream of the KNOX/BELL system in liverworts.