The epigenome and nuclear architectural mechanisms that regulate neuronal activity-induced transcriptional responses in cortical neurons remain incompletely understood. Previously, we have shown that the chromatin organizer SATB2 and the inner nuclear membrane protein LEMD2 form a chromatin tether at the nuclear lamina, and that activity-induced transcription is impaired in both Satb2 and Lemd2 loss-of-function models. Interaction of SATB2 and LEMD2 with subunits of the ESCRT-III complex indicates that the ESCRT-III complex could serve as an activity-dependent, dynamic component of this tether. Here, we study the activity-dependent subcellular localization and function of the ESCRT-III components CHMP7 and CHMP4B in primary cortical neurons. We find that increased neuronal activity correlates with the accumulation of co-localized CHMP7 and CHMP4B foci at the nuclear envelope. shRNA-mediated Chmp7 knockdown causes a reduction in the expression of activity-regulated genes and genes with highly specialized functions in synaptic organization and trans-synaptic signaling. Furthermore, the observed similarity in the global transcriptome responses in Satb2, Lemd2, and Chmp7 loss-of-function models points toward a previously unrecognized role of the SATB2–LEMD2–CHMP7 tether in linking chromatin architecture and nuclear envelope plasticity to activity-dependent gene regulation.