Land plant meristems are reservoirs of stem cells that allow directional growth in response to favourable environments. To what extent an ancestral meristem genetic program was retained by all plant lineages is yet to be determined. Diploid sporophytic meristems and their underlying gene regulatory networks have been extensively studied in model vascular plants (e.g. Arabidopsis), yet less is known about genes controlling meristem formation in bryophyte species with free-living haploid gametophytes. We show that in the liverwort Marchantia polymorpha (Marchantia), the single B-Class AUXIN RESPONSE FACTOR (MpARF2) is essential for gametophytic meristem maintenance. B-ARFs are land plant-specific transcriptional repressors, antagonists of the auxin response pathway and their expression predates meristem formation during Marchantia gemmae development. We use an inducible CRE/lox system to express and excise an artificial microRNA targeting MpARF2 (amiRMpARF2) leading to a respective loss and recovery of meristems during plastochron developmental transitions. Using multiple fluorescent markers, we characterise the role of MpARF2 in gemmae meristem establishment, thallus branching/bifurcation and regeneration. We further test the interaction of MpARF2 with auxin production and response genes to show that low auxin responses in sites of high auxin production are critical for three-dimensional meristem establishment. Even though bryophyte meristems are currently interpreted to be single-celled, B-ARFs are expressed beyond the apical/subapical cell domains, pointing at the need to further reconcile genetic and anatomical studies. Our work provides a novel mechanism for pluripotency maintenance in plants that may be independent of the CLE/CLAVATA peptide/LRR-RLK receptor system or WUSCHEL homeodomain transcription factors.