Plastic pollution caused by non-biodegradable plastics is one of the most widely discussed and notable challenges of the 21st century. Developing biodegradable plastics, such as polylactic acid (PLA), is broadly accepted as the ultimate way of alleviating this problem. However, current PLA production technology relies heavily on food-producible materials such as corn, which leads to competition for resources between material production and food supply. Carbon dioxide whose excessive emission aggravates global warming is an abundant underexplored carbon resource. Herein, we developed a cyanobacterial cell factory for the de novo biosynthesis of PLA directly from CO₂, using combinational strategies of metabolic engineering and high-density cultivation (HDC). The heterologous pathway for PLA production, which involves engineered D-lactic dehydrogenase, propionate CoA-transferase, and polyhydroxyalkanoate synthase, was introduced into Synechococcus elongatus PCC7942. Subsequently, various metabolic engineering strategies, including promoter optimization, acetyl–CoA self-circulation, and carbon-flux redirection, were systematically applied, resulting in an approximately 19-fold increase of PLA to 15.0 mg g⁻¹ dry cell weight (DCW) compared to the control. Finally, the PLA titer of 108.0 mg L⁻¹ was obtained after using the HDC strategy, approximately 270 times higher than that obtained from the initially constructed strain. Surprisingly, the molecular weight (M_w, 62.5 kDa; M_n, 32.8 kDa) of our cyanobacterial PLA is among the highest reported levels, which is superior for commercialization. This study sheds light on the prospects of autotrophic plastic production from CO₂ using cyanobacterial cell factories.