The collapse of stalled replication forks is a major driver of genomic instability. Several committed mechanisms have evolved to overcome replication stress and minimize its consequences. These pathways are particularly pertinent at repetitive regions such as telomeres. Telomeres comprise tandem repeat arrays of TTAGGG sequences at the ends of chromosomes, that must be maintained in cancer cells to confer proliferative immortality. Cancer cells that use the Alternative Lengthening of Telomeres (ALT) pathway of telomere maintenance display heightened levels of telomere-specific replication stress and are thought to co-opt stalled replication forks as substrates for break-induced telomere synthesis. FANCM is a DNA translocase that can form independent functional interactions with the BLM-TOP3A-RMI (BTR) complex and the Fanconi Anaemia (FA) core complex. We demonstrate that FANCM depletion provokes excessive ALT activity, evident by increased break-induced telomere synthesis events and the induction of ALT biomarkers without telomere lengthening. FANCM-mediated attenuation of ALT activity requires its inherent DNA translocase activity and interaction with the BTR complex, but does not require the FA core complex, indicative of FANCM functioning to restrain excessive ALT activity by ameliorating replication stress in telomeres. Finally, we demonstrate that synthetic inhibition of FANCM-BTR complex formation is selectively toxic to ALT-positive cancer cells.