The idea of building the Dimitrievsky Church belonged to the famous Altai engineer and public figure Pyotr Kozmich Frolov. In the early 19th century, he held the position of head of the Altai Cabinet of His Imperial Majesty's Court and was simultaneously the civil governor of Tomsk. The centenary of the Altai mining factories was approaching, which produced about a thousand poods of silver annually. In honor of this event, it was decided to create a unique architectural ensemble for Siberian cities. Thus, the idea of constructing Demidov Square emerged, which later travelers referred to as the "corner of Petersburg" in Barnaul. It was planned to build a mountain hospital, a school, and a almshouse in the main square of the city. Since the almshouse was to accommodate the sick and disabled, it was decided to build it together with the Church of Dimitry of Rostov.

The church was laid on August 6, 1829. Unlike other buildings on Demidov Square, its construction progressed quite quickly. On August 24, 1830, Archimandrite Makary Glukharev, the founder of the Altai Spiritual Mission, arrived in Barnaul. Under the vaults of the Dimitrievsky Church, he met with the academician of painting Mikhail Ivanovich Myagkov from St. Petersburg, who was working on the church's frescoes. About six months remained before the consecration, but a significant part of the work had already been completed. Makary highly appreciated the artist's work and invited him to participate in the painting of one of the future churches of the Altai Mission. Subsequently, Myagkov built and decorated the church in Ula, now Gorno-Altaisk, at his own expense. Soon, the construction of the Dimitrievsky Church was completed, and it was consecrated in 1831.

Pyotr Kozmich Frolov not only actively participated in the construction of the church but also made significant donations. He provided everything necessary for the services: vestments, icons, silver censers, crosses, chalices, candlesticks, as well as about 20 paintings on biblical themes created by artists Lafranc, Donchi, Billeart, Nicola Poussin, and others. Frolov also donated six poods of candles and three poods of incense.

In 1905, according to the project of architect Ivan Nosovich, a chapel was built next to the church, featuring a mosaic image of Christ the Savior, donated by academician A.N. Frolov. The floor of the chapel was also made of mosaic.

In the 1920s, the church was closed, and its building was successively used as a cinema, circus, and sports hall, which contributed to its destruction. In 1994, the building was returned to the church. Before restoration could begin, it was long cleaned of debris. In 1996, Archpriest Nikolai Voitovich was appointed as the rector. The roof, ceilings, and walls were restored, windows and doors were installed, and the annex was renovated. In 1997, the altar in the annex was consecrated in honor of St. Nicholas the Wonderworker.

On May 19, 2009, Bishop Maxim of Barnaul and Altai consecrated the dome with the cross installed on the church. By the fall of 2012, the restoration was mostly completed, and on November 9, after a minor consecration, regular services resumed in the church.

Today, the church is a cultural heritage site of federal significance. In the altar, there is an ark containing a relic of St. Dimitry of Rostov, which is brought out every Sunday during the reading of the Akathist. The church also has a baptismal chapel in honor of St. Nicholas the Wonderworker, a youth Orthodox association "Slovo", a Sunday school, and a library.