The mammalian inactive X chromosome (Xi) is a model for facultative heterochromatin. Increased DNA compaction for the Xi, and for facultative heterochromatin in general, has long been assumed based on recognition of a distinct Barr body using nucleic-acid staining. This conclusion has been challenged by a report revealing equal volumes occupied by the inactive and active X chromosomes. Here, we use light and electron microscopy to demonstrate in mouse and human fibroblasts a unique Xi ultrastructure, distinct from euchromatin and constitutive heterochromatin, containing tightly packed, heterochromatic fibers/domains with diameters in some cases approaching that of prophase chromatids. Significant space between these packed structures is observed even within condensed regions of the Xi. Serial-section analysis also reveals extensive contacts of the Xi with the nuclear envelope and/or nucleolus, with nuclear envelope association being observed in all cells. Implications of our results for models of Xi gene silencing and chromosome territory organization are discussed.