The temple was founded in 1613 by Yamazaki Samanosuke Iemori, lord of Wakasa castle (in what is today Tottori prefecture), along with Takuho Sôrin Oshô of Daitoku-ji, on the former site of the mansion of Asano Nagamasa.
After the Yamazaki clan died out in 1657, the temple came to be associated with the Asano family of Akô in Harima province. As a result of Asano Naganori's famous attack on Kira Yoshinaka in 1701, the Asano family also came to ruin. Ôishi Kuranosuke then buried Naganori's court headdress at the temple, erected a stone over it in honor of his lord, and paid formal visits on numerous occasions.
Before 46 of the 47 ronin killed themselves in 1703, Sôgai, the abbot of Zuikôin, received their severed topknots (magé) from the Matsudaira, Hosokawa, Mizuno, and Môri families who had been entrusted with them. Returning to the capital, in accordance with the dying wish of Ôishi Kuranosuke, Sôgai enshrined their hair in a bottle or pot, burying it next to the grave of their lord Asano Naganori. A stone tower was then placed atop the site as a marker, inscribed with the names of the 46 ronin. As Terasaka Kichiemon did not commit seppuku alongside the other 46, his name was not included.
The temple was moved along with that tower to the Yamashina district of Kyoto in 1962.
- Plaque on-site at former site of Zuikô-in.