Telomeres and its associated proteins are essential for genome stability and limit the proliferative potential of cells. Cancer cells achieve replicative immortality either by re-expression of the enzyme telomerase or activation of a recombination-based mechanism called Alternative Lengthening of Telomeres (ALT). Hence, telomere maintenance is a universal hallmark of cancer and in addition telomere-driven genomic instability fuels oncogenic genomic alterations in the majority of cancers. In Previous work we had established that the zinc finger protein ZBTB48 directly binds to telomeric DNA and acts as a negative regulator of telomere length in both telomerase-positive and ALT-positive cancer cells. In the latter, ZBTB48 is particularly abundant at telomeres and its overexpression had been reported to cause rapid telomere shortening, but the exact molecular mechanism has not been definitively established. Here, we describe that ZBTB48 overexpression induces chromatin bridge formation as the primary cause of telomere attrition, eventually culminating in chromothripsis. ZBTB48-induced chromatin bridge formation is exclusive to ALT-positive cellular contexts, dose-dependent and leads to concomitant C-circle accumulation while the bridges persist for hours into interphase as observed by live cell imaging. Using ZBTB48 separation-of-function mutants, we profiled both proximity partners and protein interactions contributing to the chromatin bridge formation by BioID as well as locus-specific CasID coupled to label-free quantitative mass spectrometry. Our data encourage how ZBTB48-dependent recruitment of epigenetic remodelling complexes causes chromatin bridge formation as a driver for genomic instability unique to ALT-positive contexts.