A church is known to have stood in Vimmerby by the mid-1200s, when a priest named Henricus Erici is recorded in 1253. It may have existed even earlier, since the font kept in the church today dates from the late twelfth century. Records suggest the town's medieval wooden church was at some point replaced in stone, and later, in 1685, by a so-called Caroline-era church, of which a photograph survives.
By the mid-nineteenth century both that church and its bell tower needed repair, and after prolonged local debate a new building was commissioned on the same site. Designs by master builder J. Jonsson of Linköping were approved in 1851, though building work was delayed by bad weather and a low winning tender that left the builder in financial difficulty. Construction finally began in earnest in 1854, with each working day reportedly opening and closing with prayer. While the old church was being demolished, services were held outdoors in the town square. Sources differ slightly on the completion date: one account gives 1855, while a more detailed narrative describes the church as substantially finished by autumn 1857 and formally consecrated only on 4 September 1859, the dedication performed by a provost rather than the diocesan bishop, who was then of advanced age.
The church is built in a restrained neoclassical style, with a low nave and a west tower whose lantern carries a clock added in 1876, a gift from the local spirits company. An inscription over the entrance dates the building to the reign of King Oscar I, though this has been treated with some scepticism locally.
Among the furnishings, the granite font — possibly of Danish origin — is the oldest object in the church, carved around 1200. The pulpit was made in 1713 by the sculptor Olof Wiström, and the altarpiece, painted in 1877 by Sven Alfred Thörne, depicts the Transfiguration and is a copy of an altarpiece by Fredric Westin in Sankt Jacobs kyrka in Stockholm.
The church has had a succession of organs since the late seventeenth century; the present main organ was built in 1956 by the Danish firm Marcussen & Søn, incorporating an older façade from 1769, with a further chancel organ added in 1977.
The churchyard has a literary connection: it was here that Astrid Lindgren reportedly came across a gravestone commemorating two young brothers who died in 1860, an encounter said to have inspired her novel The Brothers Lionheart.