After the baptism of the Murom people, the righteous prince Konstantin began the construction of churches in the city. One of them, dedicated to the passion-bearers Boris and Gleb, according to legend, was built on the site of the current Trinity Monastery. The exact date of the replacement of the wooden Boris and Gleb church with the wooden Trinity church is unknown, but it is mentioned in the 1624 Census Book: "Opposite the Annunciation Monastery stands a wooden church of the Life-Giving Trinity with a tented top, a porch, a white iron cross and dome, as well as an altar dedicated to Boris and Gleb. The church contains icons, candles, church vessels, and vestments, and bells hang in the belfry. All this was built with the funds of the Murom merchant Boris, son of Semyon, and his son Bogdan." These merchants, known as Tsvetnovs, traded in Moscow goods, including paints, and lived nearby the Trinity church, providing support and becoming its benefactors.

In 1642, Bogdan Tsvetnov laid the foundation for the stone Trinity church on the site of the wooden one. The construction lasted about a year, as evidenced by the inscription on the wall of the church: "In 1642, on August 21, the construction of this church began. Completed on August 6, 1642, through the efforts and funds of the merchant Tarasiy, son of Bogdan Tsvetnov, for the glory of the Father, the Son, and the Holy Spirit." After the completion of the construction, Tarasiy Tsvetnov appealed to the Ryazan bishop Moisey with a request to establish a women's monastery at the site of the Trinity parish, offering to donate his yard for this purpose and to buy out the neighboring plot. The bishop supported this initiative, and Tsvetnov moved the Prechisten church to free up space for the monastery. It is likely that Tarasiy later withdrew to the neighboring Annunciation Monastery. The monastery he founded continued to develop, attracting new benefactors, and in 1663 received the peasant yards by royal decree.

In 1921, the Trinity Monastery was closed, and its buildings were left unattended, leading to their desolation. From 1933, the monastery was used by the military, and its premises served as warehouses. In 1936, some altars were dismantled, and the materials were used for the construction of a school. From 1941, the former Trinity Cathedral housed the Kрупская Artel, which was engaged in shoemaking. After the war, the monastery was converted into communal apartments. In the 1970s, its ensemble was placed under state protection as a monument of republican significance and underwent cosmetic repairs.

On May 15, 1991, the Trinity Monastery was handed over to the Church, becoming the first revived women's monastery in the Vladimir diocese. At the end of May, the first residents arrived from the Riga Trinity-Sergius Monastery. The first liturgy took place on May 26 in the Kazan church at the gate. The minor consecration of the Trinity Cathedral occurred on July 21. The church has been fully restored, although some changes in its appearance are a matter of debate. From 2008 to 2011, frescoes were completed in the cathedral. The crosses on the domes of the cathedral, crafted by Murom blacksmiths in the 17th century, were restored in the 1990s. The main relic of the cathedral and the monastery is the relics of Prince Peter and Princess Fevronia, as well as the Vilnius cross-reliquary, which appeared in Murom in 1658.