SMARCA4 encodes one of two mutually exclusive ATPase subunits in the BRG/BRM associated factor (BAF) complex that is recruited by transcription factors (TFs) to drive chromatin accessibility and transcriptional activation. SMARCA4 is among the most recurrently mutated genes in human cancer, including ∼30% of germinal center (GC)-derived Burkitt lymphomas. In mice, GC-specific Smarca4 haploinsufficiency cooperated with MYC over-expression to drive lymphomagenesis. Furthermore, monoallelic Smarca4 deletion drove GC hyperplasia with centroblast polarization via significantly increased rates of centrocyte recycling to the dark zone. Mechanistically, Smarca4 loss reduced the activity of TFs that are activated in centrocytes to drive GC-exit, including SPI1 (PU.1), IRF family, and NF-κB. Loss of activity for these factors phenocopied aberrant BCL6 activity within murine centrocytes and human Burkitt lymphoma cells. SMARCA4 therefore facilitates chromatin accessibility for TFs that shape centrocyte trajectories, and loss of fine-control of these programs biases toward centroblast cell-fate, GC hyperplasia and lymphoma. Display omitted •Smarca4 is a haploinsufficient tumor suppressor in B cells•Partial, but not complete, loss of Smarca4 drives germinal center hyperplasia•Smarca4 loss biases centrocyte cell fate toward dark zone recycling•BCL6-antagonistic TFs SPI1, IRF4, and NF-κB have reduced activity following Smarca4 loss Deng et al. identify a germinal center-specific role for SMARCA4 (BRG1) in regulating centrocyte cell fate decisions by facilitating chromatin accessibility in association with SPI1 (PU.1) and IRF transcription factors. Loss of Smarca4 partially phenocopies BCL6 activation and cooperates with MYC over-expression to drive lymphomagenesis.