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Flowers are a key reproductive innovation of the angiosperms. Seed plant reproductive axes (including flowers) evolved as reproductively specialized shoots of the land plant diploid sporophyte, with the gamete-producing haploid gametophyte becoming reduced and enclosed within ovules and microsporangia. The transcription factor LEAFY (LFY) initiates floral development, yet it predates flowers and is found across all land plants. LFY function outside angiosperms is known from the moss Physcomitrium patens, where it controls the first cell division of the sporophyte, and from the model fern Ceratopteris richardii, a seedless vascular plant where CrLFY1 and CrLFY2 maintain vegetative meristem activity. However, how LFY’s floral role evolved remains unclear. Using over-expression, we uncover new roles for CrLFY1/2 in fern gametophyte reproduction, in sperm cells and in the gametophyte's multicellular notch meristem. While no sporophytic reproductive function was detected in terms of time to sporing, over-expression supports a role in frond compounding and in the zygote's first cell division. Our findings suggest a potentially ancestral LFY function in fern haploid-stage reproduction, which might have been co-opted into the sporophyte during the origin of the flower.