Homeostatic synaptic plasticity (HSP) is an important mechanism attributed with the slow regulation of the neuron’s activity. Whenever activity is chronically enhanced, HSP weakens the weights of the synapses in the dendrites and vice versa. Because dendritic morphology and its electrical properties partition the dendritic tree into functional compartments, we set out to explore the interplay between HSP and dendritic compartmentalization. For this purpose, we used a detailed model of a CA1 pyramidal neuron receiving a large number of activity-dependent plastic synapses and developed a novel approach for specifying functional dendritic subunits. We found that the degree of dendritic compartmentalization and the location-specificity of HSP are strongly tied. A local HSP mechanism, operating at the level of the individual synapse, will regard the neuron as a multiunit distributed system, each unit consisting of many synapses, and will thus support dendritic compartmentalization, whereas a global HSP mechanism, modifying all synapses in unison, will treat the neuron as a single centralized unit. Both local and global HSP can successfully counterbalance persistent, cell-wide perturbations of dendritic activity. The spatial distribution of synaptic weights throughout the dendrites will markedly differ under the local versus global HSP mechanisms. We suggest an experimental paradigm to unravel which type of HSP mechanism operates in the dendritic tree. The answer to this question will have important implications to our understanding of the functional organization of the neuron.