<p>Cyanobacteria are photosynthetic microorganisms that can fix CO₂ via the Calvin–Benson–Bassham cycle and store carbon as glycogen, which is subsequently catabolized through multiple pathways. Unicellular cyanobacteria such as <i>Synechocystis</i> sp. PCC 6803 possess a unique tricarboxylic acid (TCA) cycle, lacking 2-oxoglutarate dehydrogenase, and excrete various low-molecular-weight carboxylic acids under dark, anaerobic conditions. Fumarate, which is a TCA cycle metabolite widely used in food additives and bioplastics, has been produced at titers below 120&#xa0;mg/L in cyanobacteria, thereby limiting its industrial potential. Here, we established high-density cultivation of genetically engineered <i>Synechocystis</i> sp. PCC 6803 and characterized a mutant lacking fumarase (Δ<i>fumC</i>), an enzyme that catalyzes the reversible conversion of fumarate to malate in the TCA cycle. The Δ<i>fumC</i> mutant exhibited increased photosynthetic activity and grew comparably to the wild-type strain under high-density conditions. The Δ<i>fumC</i> strains were cultivated at high density in nutrient-enriched BG-11 media (5 × , 10 × , and 15 ×) under 1% CO₂ and 300&#xa0;μmol photons/m²/s, resulting in fumarate production of up to 1.7&#xa0;g/L fumarate under these conditions. Furthermore, the combination of <i>fumC</i> knockout with <i>ppc</i> overexpression (encoding phosphoenolpyruvate carboxylase) enabled fumarate production at the highest titer reported to date (&gt; 2&#xa0;g/L) under photoautotrophic conditions. This study highlights the effectiveness of metabolic engineering combined with cultivation optimization to overcome the intrinsic bottlenecks in cyanobacterial carboxylic acid production, providing a promising platform for sustainable bioproduction from CO₂.</p>