Zhabdrung Ngawang Namgyel laid the foundation stone of Wangdue Phodrang Dzong in 1638, and for the next year and a half, Ponlop Nyama Kukye oversaw the construction process. The four storied tower was attributed to Zhabdrung himself, whereas in 1683, Dzongpon (regional governor) Dedun Chophel extended the upper dzong and the shabkor. A cantilever bridge built in 1685 to span the Puna Tsang Chu. In 1667, the Seventh Wangdue Dzongpon Sonam Lhundrub extended the dzong to provide a new entrance to the Jowo Lhakhang. Over time the complex grew to house over thirteen shrines and three courtyards in the complex. An image of Mahakala that was brought from Druk Lhamoche in Ralung occupies the gonkhang.
Wangdue Phodrang Dzong was impacted by a fire in 1837 and an earthquake in 1897; it was completely razed by a fire on June 24, 2012.