His Fabian strategy of wearing down the English while avoiding major battles allowed the French to recapture most of what they had lost earlier in the war.
He initially served Charles of Blois in the Breton War of Succession (1341-1364). Charles was supported by the French crown, while his rival, Jean de Montfort, was allied with England. Du Guesclin was knighted in 1354 while serving Arnoul d'Audrehem, after countering a raid by Hugh Calveley on the castle of Montmuran. In 1356-1357, Du Guesclin defended Rennes against an English siege by Henry of Grosmont, using the guerrila tactics that were to become his trademark. Though the siege was ended by payment of 100,000 crowns, the brave resistance helped restore French pride after Poitiers, and du Guesclin came to the attention of the Dauphin Charles.
When he became King in 1364, Charles sent Du Guesclin to deal with Charles II of Navarre, who hoped to claim the Duchy of Burgundy, which Charles hoped to give to his brother, Philip. On 16 May, he met Navarrese forces under the command of Jean de Grailly, Captal de Buch at Cocherel and proved his ability in pitched battle by routing the enemy. The victory forced Charles II into a new peace with the French king, and secured Burgundy for Philip.
On September 29, 1364, at the Battle of Auray, du Guesclin and Charles of Blois were heavily defeated by John V, Duke of Brittany and the English forces under Sir John Chandos. Charles was killed in action, ending the Blois pretensions in Brittany. Du Guesclin was captured and ransomed by Charles V for 100,000 francs.
In 1366, the King placed him at the head of the "free companies," the marauding soldiers who pillaged France after the Treaty of Brétigny, and sent him to Spain to aid Henry of Trastamara against Pedro the Cruel. Though successful in the campaign of 1366, Henry's army was defeated 1367 by Pedro's forces, now commanded by Edward, the Black Prince, at Nájera. Du Guesclin was again captured, and again ransomed by Charles V, who considered him invaluable. In 1369, Henry of Trastamara won the battle of Montiel, gaining him the throne of Castile.
War with England was renewed in 1369, and Du Guesclin reconquered Poitou and Saintonge and pursued the English into Brittany from 1370 to 1374. He disapproved of the confiscation of Brittany by Charles V in 1378, and his campaign to make the duchy submit to the king was halfhearted.
An able tactician and a loyal and disciplined warrior, Du Guesclin had reconquered much of France from the English when he died of dysentery at Chateauneuf-de-Randon while on a military expedition in Languedoc. He was buried at Saint-Denis in the tomb of the kings of France. His heart is kept at the basilica of Saint-Sauveur at Dinan.
The family of du Guesclin remained in France until the French Revolution of 1789 where a number of them were guillotined and the remainder fled for their lives to England and possibly the Netherlands. Here they remained.
Because of du Guesclin's allegiance to France, 20th century Breton nationalists considered him to be a "traitor" to Brittany. During World War Two, the pro-Nazi Breton Social-National Workers' Movement destroyed a statue of him in Rennes.
Du Guesclin was one of the main characters in a trilogy of children's books ("Geef me de ruimte", 1976; "Triomf van de verschroeide aarde", 1977 and "Het rad van fortuin", 1978) by the Dutch author Thea Beckman.
Bertrand du Guesclin is also a playable character in the Age of Empires II: The Age of Kings and is portrayed as a knight on horseback.