Chimeric antigen receptor (CAR) and chimeric autoantibody receptor (CAAR) T cells are novel cellular immunotherapy strategies that have recently entered clinical practice for the treatment of malignancies and autoimmune diseases. Early expansion and long-term persistence of these genetically engineered T cells predict therapeutic efficacy, but mechanisms governing effector versus memory CA(A)RT differentiation and whether asymmetric cell division (ACD) induces differential fates in human CA(A)RTs remain unclear. Here we demonstrate that a method of target-induced proximity labeling enables the isolation of first-division proximal daughter and distal daughter CA(A)RTs. First-division daughter CA(A)RTs exhibit contrasting in vitro and in vivo phenotypes and asymmetrically distribute their surface proteome and transcriptomes that can drive diverging effector and memory fates. Proximal daughter CA(A)RTs exhibit greater energetic profiles and potent cytotoxicity consistent with an effector cell phenotype. Distal daughter CA(A)RTs exhibit greater in vivo persistence and, surprisingly, demonstrated transient potent cytolytic activity that afforded superior control of tumor outgrowth, uncovering an effector-like state in distal daughters that otherwise exhibit greater potential to form memory cells. Proximal daughters enrich in target-engaged CA(A)R molecules and proteins indicative of T cell activation and trogocytosis, while distal-daughters enrich for the endogenous T cell receptor, CD8, and naïve- and memory-associated proteins. Proximal and distal daughter cells exhibit transcriptional asymmetry and opposing transcriptional trajectories consistent with diverging effector and memory differentiation, and the asymmetry in gene abundance of fate-determining factors is established through both the uneven partitioning of pre-existing mRNA transcripts and asymmetric transcriptional regulation. Across naïve, memory, and effector surface immunophenotypes, proximal daughter CARTs utilize a core of transcription factors known to support proliferation and effector function. Conversely, distal daughter CARTs demonstrate increased activity of transcription factors known to restrain effector differentiation and promote longevity, evidenced by diminished long-term in vivo persistence and function of distal daughter CARTs after IKZF1 disruption. These studies establish ACD as a framework for understanding mechanisms of CA(A)RT differentiation and improving therapeutic outcomes.