The church was built with funds from Count Nikolai Petrovich Sheremetev between 1794 and 1801 in the classical style. The design involved Moscow architect E. Nazarov, as well as serf architects Dushkin and Andrei Mironov. There is an opinion that the luxurious colonnade of the western portico, niches with statues, and multi-figure bas-reliefs were created by the famous architect Kvarengi. The Dmitriev Church was constructed as the main temple of the Spaso-Yakovlevsky Monastery.

Count Nikolai Petrovich Sheremetev spent 55,000 rubles on the construction of the church and 10,000 rubles on its decoration. The monastery honored the memory of the benefactor, and daily early liturgies were held in the Dmitriev Church for the commemoration of the Sheremetev family.

On October 27, 1801, on the feast day of Saint Dmitry, the church founded in his honor was consecrated by Yaroslavl Archbishop Pavel. In 1804, two chapels were arranged in the refectory of this church: the right one dedicated to Saint Nicholas, the heavenly patron of Nikolai Sheremetev, and the left one consecrated in honor of the Great Martyr Dmitry of Thessalonica, the namesake saint of the Rostov saint Dmitry.

Between 1800 and 1801, commissioned by the count, the interior of the church was painted by Rostov painter, serf of the Filatyev family, Porfiry Semyonov Ryabov. The decorative painting with glue paints clearly emphasizes the architectural space of the classical church. The main part of the painting is done in grisaille technique and covers the vaults and arches with a coffered grid on a blue background. In the center of the large dome is a round ceiling with an image of the 'New Testament Trinity' against a backdrop of clouds, surrounded by angels. Around it are 12 oval medallions depicting the apostles. Between the ovals are blue stripes with stucco arabesque ornamentation painted in white and black. On the sails of the vault are stucco ovals with images of the evangelists, and between them, the heads of churches.

The decorative wall adornments were updated with oil paint in 1869-1870 at the request of Count Dmitry Nikolaevich Sheremetev. The work was carried out by Alexei Nikolaevich Bubnov.

The walls are decorated with columns and pilasters made of gray artificial marble. On the southern wall are depicted Saint Dmitry of Rostov and Saint Sergius of Radonezh, on the northern, Saint Hilarion the Great and Saint Martyr Alexandra. In the apse of the central altar is depicted the 'New Testament Trinity', above the altar window, 'Savior on the Cloth', on the northern wall of the altar, Moscow metropolitans, and on the southern, universal saints. Above the western entrance to the church is depicted the scene 'The Tonsure of Saint Dmitry of Rostov'.

The preserved iconostasis opens into the altar with a wide arch. It is adorned with emerald-green pilasters with gilded capitals and is topped with a pediment. The iconostasis contains two oil-painted icons: on the left, 'The Mother of God', on the right, 'Savior on the Throne'. The design of the iconostasis made of 'fake marble' was developed by Konstantin Alexandrovich Dokushevsky. The marble work was done by Moscow master Adrian Stepanov Remizov, the carved capitals by carpenter Vladimir Lavrentyev from the village of Smertino in Rostov district, gilding by Vasily Sergeev Nesterov from the Moscow guild, and the 'marble-like' painting by Rostov merchant Ilya Nikolaev Bubnov. The icons of the original iconostasis have been preserved, painted by Nikolai Tyapin from the Moscow region. In the corner projections of the central iconostasis are his icons: on the eastern side, 'Saint Dmitry' and 'Saint Jacob' on wood, and on the western, 'Saint Nicholas the Wonderworker' and 'Saint Martyr Paraskeva' on canvas. The latter are named after Count and Countess Sheremetev.

By the southern wall of the church is a white marble canopy, installed in 1909-1910 over the remains of Metropolitan Dmitry. The relics were kept in the cathedral annually from May 25 to October 28. The upper part of the canopy is decorated with a bas-relief depicting an archbishop's mitre, two crossed candlesticks, and two laurel branches. The inscription on the canopy reads: 'Saint Father Dmitry, pray to God for us'.

The external and internal stucco work of the Dmitriev Church was done by a German master, a native of Dresden, Ivan Fohta, and in the late 1860s and early 1870s, it was updated by a master from Kostroma province, Yevgraf Vasilyev Isakov.