Triggering apoptosis remains an efficient strategy to treat cancer. However, apoptosis is no longer a final destination since cancer cells can undergo partial apoptosis without dying. Recent evidence shows that partial mitochondrial permeabilization and non-lethal caspase activation occur under certain circumstances, although it remains unclear how failed apoptosis affects cancer cells. Using a cancer cell model to trigger non-lethal caspase activation, we find that melanoma cancer cells undergoing failed apoptosis have a particular transcriptomic signature associated with focal adhesions, transendothelial migration, and modifications of the actin cytoskeleton. In line with this, cancer cells surviving apoptosis gain migration and invasion properties in vitro and in vivo. We further demonstrate that failed apoptosis-associated gain in invasiveness is regulated by the c-Jun N-terminal kinase (JNK) pathway, whereas its RNA sequencing signature is found in metastatic melanoma. These findings advance our understanding of how cell death can both cure and promote cancer. Display omitted •Pro-apoptotic BH3-only proteins and chemotherapy can trigger failed apoptosis•Melanoma cells undergoing failed apoptosis are more invasive in vitro and in vivo•This pro-invasion program is regulated by JNK-AP1•The failed apoptosis gene signature can discriminate metastatic melanoma Apoptosis is considered a complete event, efficiently killing cancer cells. Here, Berthenet et al. show that suboptimal apoptotic triggers can induce failed apoptosis, a process that enhances melanoma cancer cell aggressiveness. Moreover, failed apoptosis has a specific transcriptional signature regulated by JNK, which is enriched in metastatic melanoma.