The first part of his rule was tainted by the Breton War of Succession, fought by his father against his cousin Joanna of Penthièvre and her husband Charles of Blois.

Faced with the defiance of the Breton nobility, John IV was unable to muster military support against King Charles V, who took the opportunity to exert pressure over Brittany.

An English army under Thomas of Woodstock, 1st Duke of Gloucester, landed at Calais and marched towards Nantes to take control of the city.

However, John IV subsequently reconciled with the new French king, Charles VI of France, and paid off the English troops to avoid a confrontation.

He ruled his duchy thereafter in peace with the French and English crowns for over a decade, maintaining contact with both, but minimizing open links to England.

Between 1380 and 1385, John IV built the Château de l'Hermine (Castle of Hermine) in Vannes, which became a defensive fortress and dwelling for the Dukes of Brittany.

In 1397, Duke John IV finally managed to extricate Brest from English control by using diplomatic pressure and financial inducements.

After his death, she served as Regent to their son, John V, Duke of Brittany, and eventually married King Henry IV of England.