The original medieval church at Runsten was a so-called 'klövsadelskyrka', a distinctive double-towered form with a nave and eastern apse chancel, thought to date from around the first half or middle of the 1100s, though this is not certain since the foundations have never been archaeologically excavated. Over the following centuries it was extended and strengthened: a western tower was added in the later 1100s, the chancel walls were reinforced and a second tower built at the east gable in the 1200s, and by the mid-1200s the nave had been vaulted in two aisles. Mid-17th-century wall paintings once decorated the interior.
By the 1600s the church had already become too small for the parish. After a visitation in 1816, the idea of building a completely new church gained momentum, and demolition of the old building began in spring 1836 alongside construction of its replacement just to the north. Rather than following the officially approved plan, which would have retained the old east tower, an entirely new church was built without the Överintendentsämbetet's permission. The nave was completed in 1836 and the tower finished in 1838 under master builder Peter Isberg of Algutsrum; the church was consecrated in 1841.
The result is a plain, whitewashed neoclassical building with a rectangular nave, tall round-arched windows, and a tiled roof that is hipped over the sacristy. The tower, clad in copper, is topped by an octagonal lantern. The exterior has remained largely unchanged since the 1830s, apart from a sacristy doorway opened in 1962.
Several older furnishings survive from the earlier church, most notably a sandstone font dated to around 1225 and an enamelled crucifix made in Limoges in the early 1200s. A runic stone is built into the sacristy wall, and older grave slabs hang in the porch. Other medieval pieces recorded include a German madonna figure from the 1300s, a carved figure of a 'holy king' (possibly Saint Erik or Saint Olof) from the late 1200s, and a medieval sacrament cabinet. The altarpiece, painted in 1847, is a copy after a work in Kalmar Cathedral that itself reproduces Rubens's famous depiction of the Descent from the Cross; parts of an older 18th-century altar structure, including reliefs and small paintings, were incorporated into the new arrangement.
The church has had two organs: a thirteen-stop instrument built in 1856 by Nils Petter Petersson behind a façade designed by Johan Fredrik Åbom, and the present pneumatic organ of 18 stops built in 1935 by Olof Hammarberg of Gothenburg behind the same historic façade.