The medieval church at Listerby was a plain, tower-less building of grey stone, likely similar in form to nearby churches at Edestad and Fridlevstad. Its bells hung in a separate wooden bell frame south of the church, a type known locally as the Edestad style. A sacristy was added to the north side of the choir in 1738, and a porch had been built on at some earlier point in the Middle Ages.
By the 1840s the old church was replaced almost entirely. Working from designs attributed to a land surveyor from Ronneby, and under the supervision of a master mason from Tving, builders raised a new nave and a narrower chancel with an apse, completed in 1847–49. Only part of the old north wall and the 1738 sacristy were retained from the earlier structure. A tower, designed by the architect Johan Adolf Hawerman, was added in 1871, giving the church its present external appearance. Two bells hang in the tower: one cast in Karlskrona in 1704, the other in Malmö in 1746.
The chancel is dominated by a large mural behind the altar, painted in 1950 by the Blekinge artist Gunnar Torhamn, depicting the Resurrection of Christ. It serves in place of a conventional altarpiece. The same artist carved relief figures of the four evangelists that decorate the panels of the pulpit, a piece of oak furniture dating from around 1600 that survives from the earlier medieval church.```
The font, in sandstone with a canopy, dates from 1950 and replaced an older wooden font. A notable survival from the old church is the gallery balustrade, carved with the twelve apostles; not all the panels could be fitted onto the new organ gallery, so four of them are displayed instead in the porch.
The organ case, in white and gold, was designed in 1882 for an earlier instrument by the Åkerman & Lund firm. The organ itself was replaced in 1985 by a new instrument built by a Lund workshop, though it retains the older façade.