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SUMMARY CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptides are 12–13 amino acid‐long peptides that serve as positional signals in plants. The core CLE signaling module consists of a CLE peptide and a leucine‐rich repeat receptor‐like kinase, but in flowering plants, WUSCHEL‐RELATED HOMEOBOX (WOX) transcription factors are also incorporated to form negative feedback loops that regulate stem cell maintenance in the shoot and root. It is not known whenWOXgenes were co‐opted into CLE signaling pathways, only that mosses and liverworts do not require WOX for CLE‐regulated stem cell activities. We identified 11 CLE‐encoding genes in the Ceratopteris genome, including one (CrCLV3) most similar to shoot meristem CLE peptide CLAVATA3. We performed the first functional characterization of a fern CLE using techniques including RNAi knockdown and synthetic peptide dosage. We found that CrCLV3 promotes cell proliferation and stem cell identity in the gametophyte meristem. Importantly, we provide evidence for CrCLV3 regulation of theWOXgeneCrWOXAduring the developmental stage when female gametangium formation begins. These discoveries open a new avenue for CLE peptide research in the fern and clarify the evolutionary timeline of CLE‐WOX signaling in land plants.