During the Sengoku period, Odawara Castle had very strong defenses, as it was situated on a hill, surrounded by moats with water on the low side, and dry ditches on the hill side, with banks, walls and cliffs located all around the castle, enabling the defenders to repel attacks by Uesugi Kenshin in 1561 and Takeda Shingen in 1569.

On his death, Odawara Domain was revived as an 85,000 koku holding for Inaba Masakatsu, the eldest son of Kasuga no Tsubone, the wet nurse to Shōgun Tokugawa Iemitsu.

During the Boshin War of the Meiji restoration, Ōkubo Tadanori permitted the pro-Imperial forces of the Satchō Alliance to pass through Odawara on their way to Edo without opposition.

[2] The new Meiji government ordered the destruction of all former feudal fortifications, and in compliance with this directive, all structures of Odawara Castle were pulled down from 1870–1872.

The Imperial Villa was destroyed by the 1923 Great Kantō earthquake, which also caused many of the stone facing on the castle ramparts to collapse.

The three-tiered, five-storied donjon, the top floor of which is an observatory, was rebuilt in 1960 out of reinforced concrete to celebrate the 20th anniversary of the proclamation of Odawara as a city.

However, the reconstructed donjon is not historically accurate, as the observation deck was added at the insistence of the Odawara City tourism authorities.