Synapses are critical for plasticity and memory formation, and they are energy-intensive. Mitochondria, which provide local energy support, are stabilized near synapses via the cytoskeleton. However, the mechanisms that anchor and stabilize mitochondria to support synaptic plasticity are not well understood. This study identified proteins that specifically tether mitochondria to actin near postsynaptic spines. The vesicle-associated membrane protein-associated protein (VAP), implicated in amyotrophic lateral sclerosis, was found to stabilize mitochondria via actin near spines. To test if VAP-dependent stable mitochondrial compartments support synaptic plasticity, the authors used two-photon glutamate uncaging to induce spine plasticity and investigated the induced and adjacent uninduced spines. They found that VAP functions as a spatial stabilizer of mitochondrial compartments for up to ~60 minutes and as a spatial ruler determining the ~30 μm dendritic segment supported during synaptic plasticity. The study also revealed that VAP is expressed as two paralogs, Vapa and Vapb, with Vapb specifically enriched near dendritic mitochondria. Deletion of VAP affected the sustained morphological plasticity in induced spines and adjacent spines within 30 μm, suggesting that VAP is crucial for local energy supply and synaptic plasticity.Synapses are critical for plasticity and memory formation, and they are energy-intensive. Mitochondria, which provide local energy support, are stabilized near synapses via the cytoskeleton. However, the mechanisms that anchor and stabilize mitochondria to support synaptic plasticity are not well understood. This study identified proteins that specifically tether mitochondria to actin near postsynaptic spines. The vesicle-associated membrane protein-associated protein (VAP), implicated in amyotrophic lateral sclerosis, was found to stabilize mitochondria via actin near spines. To test if VAP-dependent stable mitochondrial compartments support synaptic plasticity, the authors used two-photon glutamate uncaging to induce spine plasticity and investigated the induced and adjacent uninduced spines. They found that VAP functions as a spatial stabilizer of mitochondrial compartments for up to ~60 minutes and as a spatial ruler determining the ~30 μm dendritic segment supported during synaptic plasticity. The study also revealed that VAP is expressed as two paralogs, Vapa and Vapb, with Vapb specifically enriched near dendritic mitochondria. Deletion of VAP affected the sustained morphological plasticity in induced spines and adjacent spines within 30 μm, suggesting that VAP is crucial for local energy supply and synaptic plasticity.