Cancer is one of the leading cause of mortality worldwide. Current anti-cancer therapeutics are approved for specific targets (e.g., ER, RAS, HER2). Despite initial favorable responses, cancer cells still acquire drug resistance and cross-tolerance to other treatments overtime. To address this urgent unmet need, new targets must be identified. Our research focuses on Chaperonin-containing TCP-1 (CCT), a double-ring, cylindrical protein folding complex consisting of eight subunits. Cancer patient databases revealed that higher gene expression of the second subunit, CCT2, correlates with tumor progression and poorer survival probability across various cancers. We hypothesize that cancer cells upregulate CCT2 to meet the demand for increased protein folding activity to produce essential products resulting from genomic alterations. Functionally, the depletion of CCT2 decreased cell viability and proliferation in T47D (luminal A breast cancer) cells and reduced tumor growth, nodule amounts, and CCT2 RNA in S-K-NAS (non-MYCN amplified neuroblastoma) tumors subcutaneously injected in nude mice. Conversely, the exogenous expression of CCT2 in T47D cells caused changes in cytoskeletal morphology (e.g. increased F-actin staining), greater migration, and larger sized spheroids compared to control cells. Through transcriptomic analysis, we found that depletion of CCT2 caused different patterns of transcriptomic changes in T47D compared to S-K-NAS cells, but showed similarities in decreased mRNA expression of other CCT subunits, molecular chaperones (e.g. HSP) and key oncogenic clients in major cancer signaling pathways. Gene ontology (GO) enrichment analysis showed that DNA processing and transcription could be implicated in breast cancer and cytoplasmic processes (e.g. protein localization, clathrin-coat assembly) are affected in neuroblastoma with CCT2 depletion. These results support that therapeutically targeting CCT for inhibition could target multiple oncogenic drivers, such as transcription factors and signaling kinases. As such, CCT inhibition could have a global impact on cancer cells without the need to pre-identify organ-specific genomic changes.