Chromosomal translocations encode oncogenic fusion proteins that have been proven to be causally involved in tumorigenesis. Our understanding of whether such genomic alterations also affect non-coding RNAs is limited, and their impact on circular RNAs (circRNAs) has not been explored. Here, we show that well-established cancer-associated chromosomal translocations give rise to fusion circRNAs (f-circRNA) that are produced from transcribed exons of distinct genes affected by the translocations. F-circRNAs contribute to cellular transformation, promote cell viability and resistance upon therapy, and have tumor-promoting properties in in vivo models. Our work expands the current knowledge regarding molecular mechanisms involved in cancer onset and progression, with potential diagnostic and therapeutic implications. Display omitted •F-circRNAs are generated from cancer-associated chromosomal translocations•F-circRNAs promote transformation and cell survival upon treatment•F-circRNAs confer resistance to treatment in tumor cells Chromosomal translocations associated with cancer give rise to fusion circRNAs which contribute to cellular transformation, affect cell viability, and have tumor-promoting properties in in vivo models.