The church forms the palace's north tower and has origins in the reign of Queen Hedvig Eleonora, with initial designs by Nicodemus Tessin the Elder, later completed by his son Nicodemus Tessin the Younger. Construction began in 1696, though the building was not finished until 1728, with interior work following under the direction of Carl Hårleman. The church was consecrated in 1730, remodelled in 1740, and re-consecrated in 1746, by which time Drottningholm had passed to Princess Lovisa Ulrika of Prussia as a wedding gift on her marriage to the future King Adolf Fredrik.
The building is circular, with three slightly projecting central sections, and is crowned by a copper-clad dome fitted with windows and a lantern. A south-facing entrance from the church hall leads directly into the palace itself, while the main entrance faces the garden to the west.
A freestanding bell tower was erected nearby in 1698 to house two bells cast at the Meyer foundry, though these were later moved to a new bell tower on Flaggberget when the palace theatre was built in the 1760s.
Inside, the altar is positioned facing the royal gallery, an arrangement that reflects the church's courtly function. The pulpit cloth is said to have been embroidered by King Gustaf V, and the altarpiece was painted by court painter G.E. Schröder. The open pew arrangement with its east–west central aisle dates from the early twentieth century.
The church has had a succession of organs, beginning with a seventeenth-century instrument and followed by one built in 1730 by Johan Niclas Cahman, paid for by Queen Ulrika Eleonora; the organ has since been altered and rebuilt several times.