Neuronal activity rapidly reprograms dendritic translation via eIF4G2:uORF binding. This study investigates how depolarization affects local dendritic biology by monitoring changes in dendritic protein expression and mRNA regulation. Depolarization of primary cortical neurons with KCl or the glutamate agonist DHPG caused rapid reprogramming of dendritic protein expression, where changes in dendritic mRNAs and proteins are weakly correlated. For a subset of pre-localized messages, depolarization increased the translation of upstream open reading frames (uORFs) and their downstream coding sequences, enabling localized production of proteins involved in long-term potentiation, cell signaling, and energy metabolism. This activity-dependent translation was accompanied by the phosphorylation and recruitment of the non-canonical translation initiation factor eIF4G2, and the translated uORFs were sufficient to confer depolarization-induced, eIF4G2-dependent translational control. These studies uncovered an unanticipated mechanism by which activity-dependent uORF translational control by eIF4G2 couples activity to local dendritic remodeling. The complex and highly elongated structure of neurons renders subcellular regions subject to local demands. mRNA localization in neurites is thought to play a critical role in neuronal homeostasis and synaptic plasticity, and activity-dependent changes in translation are required to drive synaptic plasticity, learning, and memory. However, with current molecular tools, the dynamics of synaptic metabolism and molecular plasticity are not fully understood. Imaging approaches established the groundwork for the discovery of mRNAs in neurites. The subcellular localization and translation of these RNAs have been studied using mechanical separation methods. Enzymatic tagging has recently enabled the cell-type-specific analysis of protein composition of subcellular compartments. Studies in resting neurons revealed the unique biology of localized transcripts, their isoform specificity, and 5' and 3' untranslated region (UTR) regulation by RNA-binding proteins (RBPs). Dendritically localized RNAs, for example, have longer 5' UTRs, which can enable complex translational programs by forming structural motifs and interacting with RBPs. Association of these RBPs with 5' UTRs correlates with the translation dynamics of neuronal transcripts. Sequence elements within the 5' UTRs impact ribosome engagement and translation of the downstream coding sequence (CDS) in response to different stimuli and cellular states. However, it is not known if and how 5' UTRs or other mechanisms modulate CDS translation of dendritically localized messages. A longstanding goal in neuroscience is to understand how the localization of dendritic RNAs leads to protein synthesis-dependent synaptic plasticity. In the present study, we developed proximity-based labeling methods to simultaneously isolate dendritic RNAs and their bound regulatory proteins, along with dendritic ribosomes and proteins, to investigate how neuronal depolarization impacts molecular events in synapses. We localizedNeuronal activity rapidly reprograms dendritic translation via eIF4G2:uORF binding. This study investigates how depolarization affects local dendritic biology by monitoring changes in dendritic protein expression and mRNA regulation. Depolarization of primary cortical neurons with KCl or the glutamate agonist DHPG caused rapid reprogramming of dendritic protein expression, where changes in dendritic mRNAs and proteins are weakly correlated. For a subset of pre-localized messages, depolarization increased the translation of upstream open reading frames (uORFs) and their downstream coding sequences, enabling localized production of proteins involved in long-term potentiation, cell signaling, and energy metabolism. This activity-dependent translation was accompanied by the phosphorylation and recruitment of the non-canonical translation initiation factor eIF4G2, and the translated uORFs were sufficient to confer depolarization-induced, eIF4G2-dependent translational control. These studies uncovered an unanticipated mechanism by which activity-dependent uORF translational control by eIF4G2 couples activity to local dendritic remodeling. The complex and highly elongated structure of neurons renders subcellular regions subject to local demands. mRNA localization in neurites is thought to play a critical role in neuronal homeostasis and synaptic plasticity, and activity-dependent changes in translation are required to drive synaptic plasticity, learning, and memory. However, with current molecular tools, the dynamics of synaptic metabolism and molecular plasticity are not fully understood. Imaging approaches established the groundwork for the discovery of mRNAs in neurites. The subcellular localization and translation of these RNAs have been studied using mechanical separation methods. Enzymatic tagging has recently enabled the cell-type-specific analysis of protein composition of subcellular compartments. Studies in resting neurons revealed the unique biology of localized transcripts, their isoform specificity, and 5' and 3' untranslated region (UTR) regulation by RNA-binding proteins (RBPs). Dendritically localized RNAs, for example, have longer 5' UTRs, which can enable complex translational programs by forming structural motifs and interacting with RBPs. Association of these RBPs with 5' UTRs correlates with the translation dynamics of neuronal transcripts. Sequence elements within the 5' UTRs impact ribosome engagement and translation of the downstream coding sequence (CDS) in response to different stimuli and cellular states. However, it is not known if and how 5' UTRs or other mechanisms modulate CDS translation of dendritically localized messages. A longstanding goal in neuroscience is to understand how the localization of dendritic RNAs leads to protein synthesis-dependent synaptic plasticity. In the present study, we developed proximity-based labeling methods to simultaneously isolate dendritic RNAs and their bound regulatory proteins, along with dendritic ribosomes and proteins, to investigate how neuronal depolarization impacts molecular events in synapses. We localized