Eventually, the chateau was seized by King François I for unpaid debts to the Crown, and after François' death, King Henri II offered the chateau as a gift to his mistress, Diane de Poitiers who became fervently attached to the chateau and its view along the river. She would have the arched bridge constructed, joining the chateau to its opposite bank. She then oversaw the planting of extensive flower and vegetable gardens along with a variety of fruit trees. Set along the banks of the river, but buttressed from flooding by stone terraces, the exquisite gardens were laid out in four triangles. After King Henri died, his widow, the strong-willed Catherine de Medici, had Diane de Poitiers removed to the Chateau Chaumont. Queen Catherine made it her own favorite residence, adding a series of gardens as well.
As Regent of France, Catherine would spend a fortune on the chateau and on spectacular nighttime parties. In 1560, the first ever fireworks display seen in France took place during the celebrations marking the ascension to the throne of Catherine's son François II. On Catherine's death the chateau went to her daughter-in-law, Louise de Lorraine, wife of King Henri III. At Chenonceau Louise was told of her husband's assassination and she fell into a state of depression, spending the remainder of her days wandering aimlessly along the chateau's vast corridors dressed in mourning clothes amidst somber black tapestries stitched with skull and crossbones.
Another mistress took over in 1624, when Gabrielle d'Estrée, the favourite of King Henri IV, inhabited the castle. After that, Chenonceau was abandoned to a forlorn darkness for more than a hundred years until a wealthy noble bought it in 1732. George Sand's grandmother, Madame Dupin, saved it from destruction during the French Revolution. She was able to preserve it from being destroyed by the Revolutionary Guard because it was essential to travel and commerce being the only bridge across the river for many miles.
In 1864, Daniel Wilson, a Scotsman who had made a fortune installing gaslights throughout Paris, bought the chateau for his daughter. In the tradition of Catherine de Medici, she would spend a fortune on elaborate parties to such an extent that her finances were depleted and the chateau was seized and sold to an American. In 1913, the Menier family, famous for their chocolates, bought the chateau and still own it to this day.
During World War I the gallery was used as a hospital ward; during the Second War it was a means of escaping from the Nazi occupied Vichy zone on one side of the River Cher to the free zone on the opposite bank.
An archictectural mixture of late Gothic and early Renaissance, Chateau Chenonceau and its gardens are open to the public. Other than the Royal Palace of Versailles, Chenonceau is the most visited chateau in France.