Updated project metadata. In this study, through computational modeling and synthetic biology tools, we identified and overcame a key flux controlling node in MEP-derived terpene biosynthesis in cyanobacteria. This strategy bypasses the limitation in traditional stepwise metabolic engineering, and led to significantly higher terpene productivity. Moreover, our results revealed photosynthesis limitations during high level of terpene production. We suggest that fine-tuning energy and reductant requirement could be a key factor in establishing a viable ‘non-native’ terpene sink in photosynthetic systems.