Telomeres are terminal TTAGGG repeats that cap chromosome ends and their shortening is the basis of replicative senescence. Cancer cells must activate a telomere maintenance mechanism (TMM) to overcome this barrier. 10-15% of cancers utilise a telomerase-independent mechanism termed Alternative Lengthening of Telomeres (ALT). Patients with ALT tumours often have a poorer prognosis compared to telomerase-positive counterparts and in need of targeted treatments. A potential target is the susceptibility of telomeres to replication stress, which ALT-cancers exploit to undergo recombinational telomere synthesis and repair. There has been mounting evidence implicating a major role for Fanconi Anemia (FA) pathway proteins at telomeres. The FA pathway is canonically required for inter-strand cross-link repair and is involved in the protection of stalled replication forks. We have identified a role for the key sensing member of the FA pathway, FANCM, in maintaining telomere integrity and regulating ALT activity. Specifically, we found that loss of FANCM induced telomere dysfunction in both ALT and telomerase cells. In ALT cells, we observed a “hyper-ALT” phenotype, characterised by a dramatic increase in telomere length heterogeneity, ALT-associated PML bodies and extrachromosomal telomeric DNA species including C-circles and G-circles. This is driven by endonuclease-mediated cleavage of stalled replication forks at telomeres and coincides with upregulation of the pRPA-S4/S8-ATR and DNA-PK DNA-damage pathways. We have further determined that the MM2 and translocase domains of FANCM are functionally required for telomere protection. Overall, we have identified a potential vulnerability of ALT cancers, through FANCM deficiency, which may be exploited in the future by synthetic lethal targeting of proteins involved in DNA-damage repair.