Close attention to the historical setting with which Castiglione frames his dialogues in The Book of the Courtier (1528) reveals that the figures of Pope Julius II and his nephew Francesco Maria della Rovere are much more central to what happens in the fiction of the text than has previously been acknowledged. Indeed, there is a thematic strand within the book that can be described as Castiglione’s Francescopaedia, his account of an idealized Francesco Maria’s education at court which resonates with Xenophon’s Cyropaedia. Witnessing this process is a group of largely silent papal courtiers who have remained at Urbino after the departure of the pope, and who serve as proxies for the absent Julius. Their presence influences the discussions of the Urbino courtiers in subtle ways which are analyzed in the present study. Recognition of this influence casts many of the book’s incidents in a new light, emphasizing their historicopolitical implications rather than their psychosocial dimensions.