Oligodendrocyte calcium signaling promotes actin-dependent myelin sheath extension. Myelin, produced by oligodendrocytes in the central nervous system (CNS), is essential for rapid nerve signaling and plays roles in learning and various CNS diseases. Myelin sheath morphology, such as length and thickness, is crucial for regulating conduction velocity. While local calcium signaling in nascent myelin sheaths has been observed and can be modulated by neuronal activity, the role of calcium signaling in sheath formation remains unclear. In this study, genetic tools were used to attenuate oligodendrocyte calcium signaling during myelination in the developing mouse CNS. Surprisingly, genetic calcium attenuation did not significantly affect the number of myelinated axons or myelin thickness. Instead, it caused myelination defects resulting in shorter, dysmorphic sheaths. Mechanistically, calcium attenuation reduced actin filaments in oligodendrocytes, and an intact actin cytoskeleton is necessary and sufficient for accurate myelin morphology. Calcium signaling is a likely candidate to regulate oligodendrocyte cell biology during myelin formation and remodeling. In other cell types, calcium signaling plays essential roles in regulating numerous cell biological processes relevant to myelination, including cytoskeletal dynamics, exocytosis, and gene expression. Several studies have focused on the roles of calcium signaling in oligodendrocytes, but fewer have focused on calcium signaling in differentiating oligendrocytes or during myelination. Calcium transients occur locally in individual, nascent myelin sheaths and can be induced by neuronal activity. In zebrafish oligodendrocytes, the pattern of local calcium transients in a nascent sheath predicts whether that sheath will elongate or retract, suggesting that calcium signaling may actively control sheath morphology. Consistent with an active role in regulating sheath elongation, whole-cell patch clamping oligodendrocytes with BAPTA to sequester intracellular calcium causes newly-formed sheaths to shorten. Here, the authors used newly-developed genetic tools—CalEx and SpiCee—to determine the role of oligodendrocyte calcium signaling during myelination of the mouse CNS. They uncovered a cellular mechanism used by oligodendrocytes to sculpt myelin sheath morphology: calcium-regulated cytoskeletal assembly in nascent sheaths. This mechanism may explain how myelin sheath geometry is precisely adjusted to neuronal properties during the development and remodeling of neural circuits. The study found that oligodendrocyte calcium signaling is dispensable for myelin initiation but is required instead to accurately sculpt the growth of myelin sheaths to achieve their normal length and morphology. Calcium signaling regulates actin filament levels in early-stage oligodendrocytes. Attenuating calcium signaling in oligodendrocyOligodendrocyte calcium signaling promotes actin-dependent myelin sheath extension. Myelin, produced by oligodendrocytes in the central nervous system (CNS), is essential for rapid nerve signaling and plays roles in learning and various CNS diseases. Myelin sheath morphology, such as length and thickness, is crucial for regulating conduction velocity. While local calcium signaling in nascent myelin sheaths has been observed and can be modulated by neuronal activity, the role of calcium signaling in sheath formation remains unclear. In this study, genetic tools were used to attenuate oligodendrocyte calcium signaling during myelination in the developing mouse CNS. Surprisingly, genetic calcium attenuation did not significantly affect the number of myelinated axons or myelin thickness. Instead, it caused myelination defects resulting in shorter, dysmorphic sheaths. Mechanistically, calcium attenuation reduced actin filaments in oligodendrocytes, and an intact actin cytoskeleton is necessary and sufficient for accurate myelin morphology. Calcium signaling is a likely candidate to regulate oligodendrocyte cell biology during myelin formation and remodeling. In other cell types, calcium signaling plays essential roles in regulating numerous cell biological processes relevant to myelination, including cytoskeletal dynamics, exocytosis, and gene expression. Several studies have focused on the roles of calcium signaling in oligodendrocytes, but fewer have focused on calcium signaling in differentiating oligendrocytes or during myelination. Calcium transients occur locally in individual, nascent myelin sheaths and can be induced by neuronal activity. In zebrafish oligodendrocytes, the pattern of local calcium transients in a nascent sheath predicts whether that sheath will elongate or retract, suggesting that calcium signaling may actively control sheath morphology. Consistent with an active role in regulating sheath elongation, whole-cell patch clamping oligodendrocytes with BAPTA to sequester intracellular calcium causes newly-formed sheaths to shorten. Here, the authors used newly-developed genetic tools—CalEx and SpiCee—to determine the role of oligodendrocyte calcium signaling during myelination of the mouse CNS. They uncovered a cellular mechanism used by oligodendrocytes to sculpt myelin sheath morphology: calcium-regulated cytoskeletal assembly in nascent sheaths. This mechanism may explain how myelin sheath geometry is precisely adjusted to neuronal properties during the development and remodeling of neural circuits. The study found that oligodendrocyte calcium signaling is dispensable for myelin initiation but is required instead to accurately sculpt the growth of myelin sheaths to achieve their normal length and morphology. Calcium signaling regulates actin filament levels in early-stage oligodendrocytes. Attenuating calcium signaling in oligodendrocy