ARID1A, a subunit of the canonical BAF nucleosome remodeling complex, is commonly mutated in lymphomas. We show that ARID1A orchestrates B cell fate during the germinal center (GC) response, facilitating cooperative and sequential binding of PU.1 and NF-kB at crucial genes for cytokine and CD40 signaling. The absence of ARID1A tilts GC cell fate toward immature IgM+CD80−PD-L2− memory B cells, known for their potential to re-enter new GCs. When combined with BCL2 oncogene, ARID1A haploinsufficiency hastens the progression of aggressive follicular lymphomas (FLs) in mice. Patients with FL with ARID1A-inactivating mutations preferentially display an immature memory B cell-like state with increased transformation risk to aggressive disease. These observations offer mechanistic understanding into the emergence of both indolent and aggressive ARID1A-mutant lymphomas through the formation of immature memory-like clonal precursors. Lastly, we demonstrate that ARID1A mutation induces synthetic lethality to SMARCA2/4 inhibition, paving the way for potential precision therapy for high-risk patients. Display omitted •ARID1A enables stepwise and cooperative chromatin binding for PU.1 and NF-kB factors•Multiome analysis shows ARID1A loss drives cell fate toward memory B cell program•ARID1A loss links memory-like FLs to higher DLBCL transformation risk in patients•ARID1A-mutant lymphoma cells show enhanced vulnerability to BAF complex inhibition Barisic et al. show a chromatin remodeling mechanism by which the BAF complex enables stepwise binding of PU.1 and NF-kB factors, thus restricting the memory B cell program and transformation to an aggressive form of lymphoma.