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Plant shoots grow from stem cells within shoot apical meristems (SAMs), which produce lateral organs while maintaining the stem cell pool. In the model flowering plant Arabidopsis , the CLAVATA (CLV) pathway functions antagonistically with cytokinin signaling to control the size of the multicellular SAM via negative regulation of the stem cell organizer WUSCHEL (WUS). Although comprising just a single cell, the SAM of the model moss Physcomitrium patens (formerly Physcomitrella patens ) performs equivalent functions during stem cell maintenance and organogenesis, despite the absence of WUS-mediated stem cell organization. Our previous work showed that the stem cell–delimiting function of the receptors CLAVATA1 (CLV1) and RECEPTOR-LIKE PROTEIN KINASE2 (RPK2) is conserved in the moss P. patens . Here, we use P. patens to assess whether CLV–cytokinin cross-talk is also an evolutionarily conserved feature of stem cell regulation. Application of cytokinin produces ectopic stem cell phenotypes similar to Ppclv1a , Ppclv1b , and Pprpk2 mutants. Surprisingly, cytokinin receptor mutants also form ectopic stem cells in the absence of cytokinin signaling. Through modeling, we identified regulatory network architectures that recapitulated the stem cell phenotypes of Ppclv1a , Ppclv1b , and Pprpk2 mutants, cytokinin application, cytokinin receptor mutations, and higher-order combinations of these perturbations. These models predict that Pp CLV1 and Pp RPK2 act through separate pathways wherein Pp CLV1 represses cytokinin-mediated stem cell initiation, and Pp RPK2 inhibits this process via a separate, cytokinin-independent pathway. Our analysis suggests that cross-talk between CLV1 and cytokinin signaling is an evolutionarily conserved feature of SAM homeostasis that preceded the role of WUS in stem cell organization.