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 On Guidobaldo's death in 1508, Castiglione continued in the service of the new duke, Francesco Maria della Rovere ("my lord Prefect" of ), who appointed him governor of Gubbio. In the following year he served in his master's campaign against the Venetians, and contracted a dangerous illness, during which he was tenderly nursed by the dowager duchess, Elisabetta Gonzaga. In 1511 he accompanied the duke to Rome on the occasion of the latter's trial for the murder of Cardinal Alidosi, and was active in Francesco Maria's successful defence. In 1513 the duke created him Count of Novillara and gave him an estate of that name, which however he soon lost through the Medici usurpation of the duchy, and never regained. At the death of Julius II, Castiglione was ambassador to the sacred college, and continued in that office during nearly the whole of Leo X's pontificate. His numerous letters show the variety and importance of the diplomatic business in which he was engaged. Several plans for his marriage came to nothing, and on one occasion, when the lady's father hesitated, the suitor broke off negotiations, saying: "The wife that I am to take, be she who she may, I desire that she should be given to me with as good will as I take her withal,— yea, if she were the daughter of a king."

Pope Leo having in 1516 basely deprived Francesco Maria of the Duchy of Urbino, Castiglione accepted an invitation to Mantua and there married Ippolita, daughter of Count Guido Torello di Montechiarugolo and Francesca Bentivoglio, a daughter of the former ruler of Bologna. This union proved exceptionally happy and was blessed by three children: a son Camillo, a 'daughter Anna, and a second daughter Ippolita, at whose birth the young mother lost her life in 1520. His son attained the age of eighty years, and is said to have been the true embodiment of the qualities described in.

Castiglione resided alternately at Mantua and at Rome, where he served as Mantuan ambassador, and where his learning, wit, taste, gentle disposition and integrity earned for him an almost unique eminence at the papal court. In 1524 he was sent by Pope Clement VII as ambassador to the Emperor Charles V (who was waging war against the French in Italy), but while his counsel and high qualities were appreciated, he was too honest a man to cope with the tortuous politics of the time, and proved unable to avert the capture and sack of Rome (1527) or the imprisonment of the pope. These catastrophes, together with a malicious and easily disproved charge of treason brought against him, preyed upon his health, and despite the many honours conferred upon him by Charles, he failed to rally, and finally died at Toledo, 7 February 1529, without again seeing his native land. His body was afterwards brought to Italy and buried in the church of the Madonna delle Grazie near Mantua, where his tomb was erected from designs by his young friend Giulio Romano.

Besides, his writings comprise: Tirsi, an eclogue of fifty-five stanzas in ottava rima, written and recited at the court of Urbino for the carnival of 1506; a prologue and epilogue for his friend Bibbiena's Calandra; a few Italian lyrics of moderate merit; and some better Latin elegies and