Poly-γ-glutamic acid (γ-PGA) is a natural polymer with diverse industrial applications. Low substrate utilization efficiency and excessive foaming during fermentation severely hindered the synthesis and application of γ-PGA. This study aimed to develop a Bacillus subtilis strain with enhanced γ-PGA production and improved carbon utilization, as well as reduced foam generation. Through the precise deletion of isocitrate lyase encoding gene aceA in γ-PGA synthesis strain B. subtilis JJ-2, a high-yield mutant JJ-2ΔaceA was established with strengthened γ-PGA production capacity. The γ-PGA yield increased to 61.35 g/L with a carbon source consumption ratio of 97.4%. Based on transcriptome and metabolome analyses, a “Block-Push-Pull” synergistic metabolic reprogramming mechanism was elucidated to explain the great improvement of γ-PGA yield. The deletion of aceA gene severed glyoxylate shunt (“Block”) and simultaneously enhanced the expression of glycolytic genes (“Push”), leading to accumulation of α-KG and L-glutamic acid precursors. The synchronous upregulation polymerase genes pgsBCA efficiently converted precursors into γ-PGA (“Pull”). A pronounced low-foam phenotype was also observed in JJ-2ΔaceA strain, which was closely associated with the global inhibition of the lipopeptide synthesis operon srfA after aceA knockout. Finally, the high productivity and foam-free phenotype was inherited and validated during fermentation with dextrin in 50 L reactor, and the γ-PGA yield was further improved to 71.45 g/L. In a word, this study presents an effective strategy for high-yield and low-cost γ-PGA production, which is beneficial to γ-PGA application and also provides a paradigm for the upgrade of other bio-manufacture processes.