Cancer therapy has improved patient outcomes markedly over the last two decades. However, cancer treatments have been shown to induce senescence in different cell types. Senescent cells secrete a distinct set of factors, collectively termed the senescence-associated secretory phenotype (SASP), which has been postulated to carry both pro- and antitumorigenic properties. Pro-tumorigenic functions of the SASP include enhancement of cancer cell proliferation, induction of epithelial-to-mesenchymal transition and increased migration. The molecular mechanisms by which the SASP regulates these pro-tumorigenic features are poorly understood. Here, we report that exposure to the SASP induces loss of epithelial markers and enhanced migration in breast cancer cells, along with limited transcriptional changes. In particular, we find that Lipocalin 2 (LCN2) is strongly upregulated upon exposure to the SASP, and its inactivation impairs SASP-induced migration. Moreover, we show that in presence of senescence-inducing stimuli, LCN2 promotes breast cancer tumor growth in vivo. Finally, we show that neoadjuvant chemotherapy treatment leads to LCN2 upregulation in residual human breast tumors, which correlates with worse overall survival. These findings provide insight into the potential of targeting LCN2 as an adjuvant therapeutic approach to prevent the emergence of aggressive relapsed breast tumors following chemotherapy.