The cathedral's construction was tied to a major relocation of Kalmar itself. After the town suffered severe damage in the Kalmar War and a later fire, defence considerations led the Council of the Realm to move the city to the more easily fortified island of Kvarnholmen. The old medieval town church was eventually demolished, its bells, silver, pulpit and organ salvaged for reuse, and building stone repurposed in the new fortifications.
Work on the new church began in 1660 under Karl X Gustaf, and it was consecrated in 1682, still unfinished, under Karl XI. It was not completed until 1703, during the reign of Karl XII, giving rise to its original name, Karls domkyrka. Tessin is said to have drawn on Roman baroque churches such as Il Gesù for the exterior design, adapting their language into a restrained Nordic idiom without a dome, built on a long cross-shaped plan with four lantern-topped corner towers crowned with gilded flame urns.
Inside, the church retains much of the character of Sweden's Age of Greatness, with whitewashed vaults, side galleries and a wealth of funerary monuments. Some eighty grave slabs from the 1600s and 1700s lie within the church, alongside numerous funerary hatchments and epitaphs from the same period. The elaborate altarpiece, completed in 1712 to a design attributed to Tessin's son, is built around a sarcophagus altar and includes a large painting thought to be by David von Krafft, believed to be a mirrored copy of a well-known French depiction of the Descent from the Cross. The baroque pulpit, thought to date from the mid-1600s and possibly a war trophy brought from elsewhere, carries carved scenes from the Passion and is supported by a carved figure of Kalmar's patron saint, Saint Christopher.
The church has undergone numerous restorations over the centuries, most recently a substantial exterior and interior campaign completed in 2011, which included re-roofing, stone conservation, regilding of the roof urns, reopening of long-blocked windows, and a new raised chancel floor. A striking ship-shaped font in grey Öland limestone, made in 1963, was moved from the chancel to the south-west end of the nave, where it now sits near the entrance area referred to as the church square.
The cathedral's large organ has a complex history of rebuilding, most recently in 2013, and reuses pipework and casework going back to an 1883 instrument, itself the third organ known to have served the building.