Principal medium spiny projection neurons (MSNs) of the striatum have long been thought to be homogeneous in their somatodendritic morphology and physiology. Recent work using transgenic mice, in which the two major classes of MSN are labeled, has challenged this assumption. To explore the basis for this difference, D₁ and D₂ receptor-expressing MSNs (D₁ and D₂ MSNs) in brain slices from adult transgenic mice were characterized electrophysiologically and anatomically. These studies revealed that D₁ MSNs were less excitable than D₂ MSNs over a broad range of developmental time points. Although M₁ muscarinic receptor signaling was a factor, it was not sufficient to explain the dichotomy between D₁ and D₂ MSNs. Reconstructions of biocytin-filled MSNs revealed that the physiological divergence was paralleled by a divergence in total dendritic area. Experimentally grounded simulations suggested that the dichotomy in MSN dendritic area was a major contributor to the dichotomy in electrophysiological properties. Thus, rather than being an intrinsically homogenous population, striatal MSNs have dichotomous somatodendritic properties that mirror differences in their network connections and biochemistry.