According to a local story, the parish priest Samuel Ödmann fell asleep while fishing and dreamed of a church for the district, waking only when his boat ran aground. Taking this as a sign of where the church should stand, he is said to have persuaded Count Anders Cederström of Beatelund to pay for its construction. The chapel, originally known as Pilhamn's chapel, was completed in 1792.
The building is a log-timber hall church with a narrower sacristy added to the east and a narrower porch to the west, standing on a fairly tall plinth of tarred rubble stone. It was later clad in standing panelling and renamed Ingarö kyrka. All parts of the building are covered by gently broken mansard roofs finished with tarred wooden shingles, and a small church jetty stands nearby, recalling the waterborne access once typical of archipelago parishes.
Inside, the pulpit is among the older furnishings and originally stood above the altar; it was moved to the north side of the east wall during a 1932 restoration, allowing access from the sacristy, and its original colours were uncovered by a conservator in 1972. The wooden font, painted with green marbling, dates from the later twentieth century. On the altar stands a crucifix made in 1959 by the sculptor Arne Jones, donated to the church in 1981. The altarpiece, depicting Christ preaching to a community of fishermen, was painted in 1952 by Einar Forseth; an earlier altarpiece, originally from Kungsholm parish in Stockholm, had hung in the church since 1907.
The church has had several organs. An 1866 instrument by Daniel Wallenström was replaced in 1923 by an organ from Åkerman & Lund, and the current mechanical organ, built by the same firm in 1980, retains an older case front.
The churchyard is the resting place of several notable Swedes, including the aviation pioneer Carl Cederström (grandson of the church's original benefactor) and his second wife Minna Poppius, the author Maj Fant, actor Georg Funkquist, opera director Göran Gentele, designer Stig Lindberg, cinematographers Sven Nykvist and Hilding Bladh, military commander Torsten Rapp, shipowner Sven Salén, and industrialist Sten Westerberg.