Machiavelli segues into a discussion of ecclesiastical principalities, which are "won by prowess or by fortune but are kept without the help of either." These states are stewarded by "religious institutions," which possess such power that regardless of the current prince's behavior or abilities, the principality remains secure. Unlike all other states, ecclesiastical princes possess a state but do not defend it and have subjects but do not govern them. Ecclesiastical principalities are largely safe from rebellions and are the only totally "secure and happy" states. Additionally, ecclesiastical states are "sustained by higher powers." Since they are "maintained by God," Machiavelli says that he will refrain from the presumptuousness of trying to fully comprehend them. Nonetheless, Machiavelli embarks on an analysis of the contemporary Roman Catholic Church's "great temporal power," which it has attained since the papacy of Alexander VI.
Machiavelli describes the solid foundations on which ecclesiastical principalities rest, rendering them virtually indestructible. Rulers of these states have an unusual relationship with their states, which function independent of rulers' prowess or fortune, and with their subjects, whom they do not govern in the typical sense. Safe from popular rebellions, ecclesiastical states possess a unique type of security, which they derive from their foundation upon religion. Machiavelli refrains from serious criticism of ecclesiastical states, chief among them the Roman Catholic Church, likely owing to the power of the Church and its pope, who was believed to be infallible.
Before Charles VIII of France invaded Italy, the peninsula was ruled by several separate states: the pope, the Venetians, the king of Naples, the duke of Milan, and the Florentines. These states had "two main preoccupations": ensuring that no foreign ruler invaded Italy and maintaining the balance of power between themselves. Two factions of Roman barons, the Orsini and Colonna, had traditionally kept the papacy weak and its power in check. Because of the "brevity" of each pope's rule, no pope had been able to crush the power of both the Orsini and Colonna until the reign of Alexander VI. Using his son, Cesare Borgia, as "his instrument" and the invasion of France as his opportunity, Alexander VI waged war and greatly enhanced the earthly power of the Church.
Using the armies and conquests of his son, Pope Alexander VI greatly enhanced the earthly power of his ecclesiastical state. With a combination of diplomacy and warfare, Alexander used his considerable prowess to expand the papacy's dominion. Alexander employed laws and arms to break the internal power of Rome's factions and to overcome the Church's outside opponents. Under Alexander's stewardship, the Church became an aggressive state with power and influence that exceeded any single pope's reign.
Following Alexander VI's death and Cesare Borgia's subsequent loss of power, the Church inherited "the fruits" of the previous pope's conquests. Pope Julius II, finding the power of the Church greatly expanded, built on the foundations of his predecessor. Julius kept the Roman barons in check and continued the wars of conquest. Julius' successor, Pope Leo, now finds the Church and papacy "in an extremely strong position." Machiavelli expresses his hope that Leo will use his "goodness and countless other virtues" to make the Church "very great and revered."
Subsequent popes benefitted from the strong foundations laid by Alexander. Machiavelli implores Leo to use his prowess as steward of the Church. Machiavelli lauds Leo, a Medici relative of the man to whom his book is dedicated, Lorenzo. Seeking to convince Lorenzo of his loyalty to the Medici, Machiavelli lavishes praise and good wishes on this other powerful member of the family.