Although the castle was designated a National Historic Site in 1931,[1] the original Tenshu and buildings were all destroyed by US bombing campaigns during the Pacific War.

Due to their strength with matchlock guns and guerrilla tactics, Nobunaga was unable to defeat the Saiga Ikki; however, the campaign was resumed by his successor, Toyotomi Hideyoshi.

With the assistance of Tōdō Takatora, who was noted for castle architecture, he began rebuilding a small fortification on Torafusayama hill which had been a relic of Hatakeyama rule, with low stone walls aligned with the natural terrain, and the central bailey located next to the current central bailey area.

[3] Asano greatly expanded Wakayama Castle, constructing a three-story tenshu connected to three corner yagura by corridors.

The overall dimensions of the castle were expanded to the northeast and the daimyō residence was relocated to this new enclosure, which was further protected by a double series of moats, utilizing the nearby Kinokawa River.

He rescued many ronin in the aftermath of the battle by hiring them for the domain and further expanded Wakayama Castle with a new northwest enclosure, and greatly strengthening its walls.

The issue was caused by the 1651 Keian Uprising in which the military strategist Yui Shōsetsu attempted to overthrow the Tokugawa shogunate and used Yorinobu's name without permission.

In 1791 the US captains John Kendrick of the Lady Washington and William Douglas of the Grace visited Kushimoto, hoping to open a trading relationship with Japan.

[4][5][6] In 1846, most of the castle was destroyed in a fire caused by lightning, but due to its special status, reconstruction of buildings including the tenshu was exceptionally permitted, and completed in 1850.