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Significance Proper elaboration of the plant body plan requires that cell division patterns are coordinated during development in complex tissues. Activation of cell cycle machinery is critical for this process, but it is not clear how or if this links to cell-to-cell communication networks that are important during development. Here we show that key cell divisions that generate the plant root are controlled by cell-to-cell signaling peptides which act through plant-specific receptor kinases to control expression of a specific cyclinD cell cycle regulatory gene. We show that cyclinD gene expression depends on both receptor signaling and the SHORT-ROOT transcription factor to ensure timely and robust cell division patterns., Cell division is often regulated by extracellular signaling networks to ensure correct patterning during development. In Arabidopsis, the SHORT-ROOT (SHR)/SCARECROW (SCR) transcription factor dimer activates CYCLIND6;1 (CYCD6;1) to drive formative divisions during root ground tissue development. Here, we show plasma-membrane-localized BARELY ANY MERISTEM1/2 (BAM1/2) family receptor kinases are required for SHR-dependent formative divisions and CYCD6;1 expression, but not SHR-dependent ground tissue specification. Root-enriched CLE ligands bind the BAM1 extracellular domain and are necessary and sufficient to activate SHR-mediated divisions and CYCD6;1 expression. Correspondingly, BAM-CLE signaling contributes to the restriction of formative divisions to the distal root region. Additionally, genetic analysis reveals that BAM-CLE and SHR converge to regulate additional cell divisions outside of the ground tissues. Our work identifies an extracellular signaling pathway regulating formative root divisions and provides a framework to explore this pathway in patterning and evolution.