Meristems in land plants share conserved functions but develop highly variable structures. Meristems in seed-free plants, including ferns, usually contain one or a few pyramid-/wedge-shaped apical cells (ACs) as initials, which are lacking in seed plants. It remained unclear how ACs promote cell proliferation in fern gametophytes and whether any persistent AC exists to sustain fern gametophyte development continuously. Here, we uncovered previously undefined ACs maintained even at late developmental stages in fern gametophytes. Through quantitative live-imaging, we determined division patterns and growth dynamics that maintain the persistent AC in Sphenomeris chinensis, a representative fern. The AC and its immediate progenies form a conserved cell packet, driving cell proliferation and prothallus expansion. At the apical centre of gametophytes, the AC and its adjacent progenies display small dimensions resulting from active cell division instead of reduced cell expansion. These findings provide insight into diversified meristem development in land plants.