Activity-driven transcription is a crucial step in neuronal plasticity processes. We found that during neuronal activation induced by the proepileptic drug kainic acid, there is a dramatic genomic redistribution of the transcriptional cofactors CBP and p300. These cofactors leave their default location at enhancer and promoter regions related with cell identity to occupy regulatory regions at activity-induced genes. In parallel with these changes, we also detect changes in the levels of H3K27ac and chromatin accessibility accordingly with the redistribution and modification of the epigenetic context. Strikingly, this dynamic change coincides with a transient halt in the transcription of hundreds of genes encoding key proteins involved in multiple neuronal functions whose expression is likely needed for identity maintenance, while genes related to the nuclear encoding of neuronal activity response, such as immediate early genes and other plasticity-related genes, increase their expression. Two transcriptional factor (TF) families are differentially bound to these regions, with neuronal identity regions being occupied by the proneural TF belonging to the Bhlh family, and the plasticity-related regions by the activity-regulated AP-1 and CREB complexes. These changes are transient and both transcription and epigenomic landscapes are recovered after a few hours. Together these results unveil an intriguing competition between neuronal identity- and plasticity-related transcription that may have important implications in neuronal plasticity and neuropathology since the repression of neuronal identity genes during longer periods of time could cause neuronal impairment or even neuronal loss.