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Abstract Collective migration of epithelial cells drives diverse tissue remodeling processes. In many cases, a free tissue edge polarizes the cells to promote directed motion, but how edge-free or closed epithelia initiate migration remains unclear. Here, we show that the rotational migration of follicular epithelial cells in theDrosophilaegg chamber is a self-organizing process. Combining experiments and theoretical modeling, we identify a positive feedback loop in which the mechanosensitive behavior of the atypical cadherin Fat2 synergizes with the rigid-body dynamics of the egg chamber to both initiate and sustain rotation. Mechanical constraints arising from cell–cell interactions and tissue geometry further align this motion around the egg chamber’s anterior–posterior axis. Our findings reveal a biophysical mechanism — combining Fat2-mediated velocity–polarity alignment, rigid-body dynamics, and tissue geometry — by which a closed epithelial tissue self-organizes into persistent, large-scale rotational migrationin vivo, expanding current flocking theories.