Transmission of polarity established early during cell lineage history is emerging as a key process guiding cell differentiation. Highly polarized neurons provide a fascinating model to study inheritance of polarity over cell generations and across morphological transitions. Neural crest cells (NCCs) migrate to the dorsal root ganglia to generate neurons directly or after cell divisions in situ. Using live imaging of vertebrate embryo slices, we found that bipolar NCC progenitors lose their polarity, retracting their processes to round for division, but generate neurons with bipolar morphology by emitting processes from the same locations as the progenitor. Monitoring the dynamics of Septins, which play key roles in yeast polarity, indicates that Septin 7 tags process sites for re-initiation of process growth following mitosis. Interfering with Septins blocks this mechanism. Thus, Septins store polarity features during mitotic rounding so that daughters can reconstitute the initial progenitor polarity. •Bipolar DRG neurons inherit cell shape from their progenitors•After mitosis, neurites form at sites of pre-mitosis progenitor processes•Septin 7 stores retracting process position and controls protrusion site inheritance Boubakar et al. report that morphological polarity of progenitors is inherited by newborn sensory neurons. Septin 7 labels the initial sites of progenitor processes during mitotic rounding and allows daughter neurons to protrude neurites from the same positions.