Circular RNAs (circRNAs) are covalently closed single stranded RNAs that are produced by RNA back-splicing. Recent profiling demonstrates that circRNA expression is cell-type specific and dysregulated in many cancers. Of the thousands of known circRNAs, only a small number have been implicated as functional. This makes circRNA a functional engima and we lack a systematic understanding of the cancer associated signaling pathways that are regulated by circRNAs. Here, we generated a pooled shRNA lentiviral library targeting the back-splice junction of 3,354 human circRNAs that are expressed at low to high levels. We used this library for loss of function proliferation screens in a panel of 18 cancer cell lines from four tissue types (colon, pancreas, skin and brain) that harbour mutations leading to constitutive activity of defined pathways (Wnt/beta-catenin or MAPK). Using this dataset, we identify pathway specific and common-essential functional circRNAs using two-class comparisons of signaling pathway active and inactive cell lines. We validated these observations with a secondary screen and uncovered a role for circSMAD2, a novel regulator of the WNT/beta-catenin pathway. Our screening and validation assays demonstrate that circSMAD2 suppression leads to reduced proliferation and increased cell death only in cancer cells that are dependent on Wnt/beta-catenin signaling. Additionally, we show that circSMAD2 knockdown results in reduced beta-catenin protein stability. Our work adds a circular dimension to the regulation of cancer signalling pathways and identifies circSMAD2 as novel therapeutic target for Wnt/beta-catenin dependent cancers.