The temple was built during the peak of the Vladimir principality by Grand Prince Vsevolod Yuryevich, known as the Big Nest, in honor of his heavenly patron, Dmitry of Thessalonica. Vsevolod, who took the name Dimitry at baptism, began construction in 1191, according to chronicle data found by Tatyana Timofeeva in the 1990s. Nikolai Voronin points to the years 1194-1197. The church was built from white limestone by Russian craftsmen. The Radziwill Chronicle states that Vsevolod created many churches, including the church of Dmitry, which he adorned with icons and frescoes. He did not attract masters from abroad but used local artisans.

In 1197, construction was completed with the installation of the icon of Dmitry of Thessalonica and a silver reliquary containing a piece of the martyr's clothing. In 1237, the cathedral suffered from the Mongol-Tatar invasion, was damaged and looted, and then burned several times in 1536, 1719, and 1760.

From 1837 to 1839, by order of Nicholas I, the cathedral was restored but lost some interesting architectural elements. During the Soviet era, it was preserved as a monument of ancient Russian art. In 1918, the cathedral hosted a Commission for the Preservation of Painting Monuments led by Igor Grabar, and in 1919, the church was closed for worship. The cathedral has been restored multiple times, and in 1999 and 2004, work was done to improve its condition.

Currently, the cathedral is managed by the Vladimir-Suzdal Museum-Reserve and functions as a museum. Worship services were not held for a long time, but in 2011, a liturgy took place in the cathedral, and it became active, remaining part of the museum-reserve and not being transferred to the Russian Orthodox Church.