Non-concentric closure of the contractile ring, known as unilateral cytokinesis, often orients along the body axis to maintain tissue integrity in various animals. Despite the identification of unilateral cytokinesis regulators, the mechanism of initial symmetry breaking remains elusive. Here, we report that intrinsic and extrinsic inhibition of cortical flow breaks cytokinesis symmetry in Caenorhabditis elegans . By coupling high-resolution 4D imaging with an in vitro cell contact reconstitution assay, we found that unilateral cytokinesis of the zygote P 0 and the two-cell stage blastomere AB are regulated by actin-dependent and adhesion-dependent mechanisms, respectively. Intracellular compression and intercellular adhesion in P 0 and AB, respectively, locally inhibit both furrow-directed cortical flow and cleavage furrow ingression, resulting in eccentric ring closure. Our study demonstrates that local mechanical suppression of ring-dependent cell cortex pulling is a common symmetry-breaking cue underlying distinct modes of unilateral cytokinesis.