Many mollusks have external, calcified shells that protect against biotic and abiotic stresses. Shells are fantastically varied in shape, size, ornamentation, and pigmentation in response to these ecological pressures. Despite this incredible diversity in shell morphology, the cellular and developmental mechanisms underlying shell growth are poorly understood. Growth and shell shape are controlled by the shell margin, a band of cells surrounding the shell opening. Here, we characterize and define Ilyanassa obsoleta’s shell margin into functional zones, each with distinctive cell morphology, function, and gene expression. Within these zones, we have discovered two zones of proliferation, as judged by EdU cell proliferation experiments. Within the first, most anterior growth zone, we find that cell divisions are strongly biased to be transverse relative to the anterior-posterior axis; this pattern of division can explain the observed circumferential expansion of the shell aperture. These divisions are left biased which is consistent with the observed higher rate of aperture expansion on the left side. In the second, more posterior growth zone, we find that cell divisions are significantly biased so they occur at an oblique angle to the right of the anterior-posterior axis. This can explain the greater aperture extension on the right side of the margin, which generates the coil of right-handed shells like Ilyanassa. These experiments describe how cellular behaviors can generate the growth patterns of gastropod shells.