In 1582, following the Honnoji Incident, Hashiba Hideyoshi took control of the capital and ordered the relocation and reconstruction of various temples as part of his urban reorganization of Kyoto. Zensoji is said to have been moved from western Kyoto to its present Sanjo-Omiya site at this time, with the monk Hoshun carrying out the relocation under Hideyoshi's orders. A temple first founded in 1542 came to its current location through Hideyoshi's reshaping of the capital — a vivid example of the urban transformation of the Azuchi-Momoyama era.

The Jizo Bodhisattva enshrined at Zensoji is traditionally said to have been carved by Dengyo Daishi Saicho himself as his personal devotional image kept throughout his lifetime. After Saicho's death it was preserved in Sakamoto in Omi Province until 1587, when the founding abbot had it installed here. Known as Mud-Foot Jizo, Sweating Jizo, and Stand-in Jizo, it is the subject of legends including helping a farmer with rice planting and saving a mother and child from a difficult birth. That the lifelong talisman of the founder of Tendai Buddhism came to reside in a Jodo-shu temple is a striking example of the unexpected crossings that mark Kyoto's religious history.