Built in 1537 by Oda Nobuyasu, the uncle of the famous warlord Oda Nobunaga, Inuyama Castle is the symbol of Inuyama City. The castle's keep is the oldest still standing in Japan, and the castle as a whole is one of only five castles to be designated a national treasure, alongside Himeji Castle, which is also registered as a World Cultural Heritage site. Built on top of a small mountain by the Kiso River, the top floor of the keep boasts a spectacular view of Inuyama City, the Kiso River, Gifu Castle, and the buildings of Nagoya Station.

Inuyama Castle was built in 1537 by Oda Nobuyasu, the uncle of Oda Nobunaga. Connected to the Nakasendo and Kisokaido roads, it was an important center throughout Japan's Warring States Period (1467-1615), located at a strategic point for trade, politics, and economics on the Kiso River. Due to its placement on the border between Owari and Mino Provinces (present-day Aichi and Gifu Prefectures, respectively), Inuyama Castle was additionally regarded as strategically vital for the capture of the country, and famous warlords such as Oda Nobunaga, Toyotomi Hideyoshi, and Tokugawa Ieyasu all made attempts to seize the castle. During the Edo Period (1603-1868), Naruse Masanari, an important vassal of the Owari Tokugawa clan, took possession of Inuyama Castle in 1617, and the Naruse clan continued to hold the castle until the end of the Edo Period. The Naruse clan modified the keep to its current form upon taking over the castle.

In 1871, the Meiji government abolished the old provinces of the Han system, replacing them with today's prefectures. Inuyama Castle became the property of Aichi Prefecture, and almost all of the buildings besides the castle keep were destroyed. In 1891, the Great Nobi Earthquake significantly damaged the remaining keep, and it was returned to the Naruse clan under the condition that they repair it. With great effort from both the Naruse clan and the citizens of Inuyama, the keep was repaired, and in 1935 it was designated a national treasure, and re-registered as such following revisions to the rules in 1952. In 2018, the old parts of the castle, from the Honmaru (inner compound) ruins to the Matsunomaru ruins and the entire Sankoji area, were designated as the Inuyama Castle Ruins National Historic Site. Until 2004, the castle was the only privately owned and preserved castle in Japan, but it is now owned by a public interest foundation established to exhibit national treasures and preserve them for future generations. Inuyama City currently manages day-to-day operations at the castle.

An elegant townscape retaining the vestiges of the days of old stretches out at the foot of Inuyama Castle. The town layout remains unchanged since the Edo Period (1603-1868), and its streets are lined with historical buildings dating from the Edo Period all the way up to the Showa Era (1926-1989). The town is home to a variety of businesses such as shops serving Gohei-mochi rice cakes, Dengaku grilled tofu, and other local delicacies, kimono rental shops, and cafes that have remodeled old machiya-style townhouses with a modern touch. In recent years, more and more shops have begun offering food that can be enjoyed while walking, making Inuyama castle town a popular tourist attraction for men and women of all ages to dress up in kimonos and walk the old-fashioned streets while savoring local dishes.