<p>Olivetolic acid (OLA), the critical aromatic precursor for plant-derived cannabinoids, conventionally relies on resource-intensive plant extraction or complex chemical synthesis. This study establishes an environmentally friendly biosynthetic platform by genetically engineering the model cyanobacterium <i>Synechocystis</i> sp. PCC 6803. We constructed the heterologous OLA pathway by co-expressing plant-derived tetraketide synthase (<i>TKS</i>), olivetolic acid cyclase (<i>OAC</i>), and acyl-activating enzyme 1 (<i>AAE1</i>). Through cultivation supplemented with sodium hexanoate, successful biosynthesis of OLA was achieved within this photosynthetic host. To overcome metabolic bottlenecks, the pathway was further optimized using the robust P_cpc560 promoter coupled with carbon sink redirection strategy. Disruption of the primary glycogen storage sink (Δ<i>glgC</i>) combined with the overexpression of the anaplerotic malic enzyme gene (<i>maeB</i>) significantly enhanced the specific OLA yield. Notably, while continuous aeration with 5% CO₂ drastically accelerated cell growth and prolonged the cultivation period, it simultaneously led to a severe decrease in the specific OLA yield. This work demonstrates the feasibility of utilizing a cyanobacterial chassis for precursor-directed OLA biosynthesis, establishing a foundational blueprint for the sustainable manufacturing of cannabinoid-related metabolites.</p>