Macrophages are important innate immune cells and key regulators of the tumor microenvironment. Due to this pivotal role, they became attractive targets for novel cell & gene therapies, including the development of genetically-engineered macrophages modified with chimeric antigen receptors (CARs). However, the efficient manufacturing of CAR-macrophages from primary sources is challenging, due to low isolation yields of primary monocytes and their resistance to traditional gene editing methods. Thus, we here demonstrate the scalable and continuous production of functional CAR-macrophages from human induced pluripotent stem cells (CAR-iMacs), showing the potential use and therapeutic impact to target CD19⁺ patient-derived cancer cells from patients with acute lymphoblastic leukemia. We successfully showed continuous CAR-iMac production of consistent quality using either small (3mL) or intermediate scale (40mL) devices showing an average yield of ~ 1×10⁷ cells/week. The generated CAR-iMacs exhibited a typical macrophage morphology and phenotype (CD45⁺, CD14⁺, CD11b⁺, CD163⁺) as well as stable CAR expression throughout the differentiation process. CAR-iMacs demonstrated enhanced phagocytosis and increased secretion of pro-inflammatory cytokines (IL-6, TNFα) against a lymphoma cancer cell line, in an antigen-dependent fashion, compared to control eGFP⁺-iMacs. Furthermore, CAR iMacs exhibited enhanced phagocytosis against primary acute lymphocytic leukemia (ALL) patient samples. scRNA sequencing revealed distinct gene expression in CAR-iMacs, compared to eGFP+-iMacs, with upregulation of genes associated with an M1 polarization, adaptive immune cell recruitment and antigen presentation. In conclusion, we present a modern, scalable and robust platform for continuous generation of functional CAR-iMacs, which opens new avenues for modern off-the-shelf immune cell-based therapies.