Admiral Stepan Makarov (commander of the Kronstadt Naval base) took control over the project and invited Vasily Kosyakov, an already renowned master of Neo-Byzantine architecture. Vasily's younger brother and partner Georgy Kosyakov was a talented graphic artist; he worked on interiors and finishes while Vasily handled overall and structural design. Makarov personally instructed Kosyakov that the cathedral must accommodate 5,000 worshippers and follow the historical Byzantine canon. In 1900–1901 Vasily Kosyakov travelled to Istanbul and Greece to refresh his understanding of genuine Byzantine art. . It is well aware that early 20th century for the Russian architecture was a time to find new ideas and forms. Contacting to Byzantine architectural heritage has been very popular among the architects of the time.

Construction of the cathedral began in 1903. By 1907, the walls and vaults were built and interior decoration began. The temple was very well equipped, electricity used for lighting and there was special boiler house for heating.

The walls of the cathedral are decorated with artificial marble. At the same time the iconostasis was made from natural stone. On the memorial plaques inside the church names of all Russian Naval officers and sailors who fallen in battles can be finded. Amazing stained glass windows of the cathedral are unique in Russia. The cathedral was consecrated in a public ceremony attended by Nicholas II and his family June 10, 1913.

The Naval cathedral operated as such for only 16 years. After the Russian Revolution it was closed and converted into a cinema house and museum. October 14, 1929 it was closed; valuables were nationalized to state treasury. A small portion of these relics were displayed at the Museum of Navy and the RussianMuseum. During World War II it was closed; the dome received three direct artillery hits. Post-war "reconstruction" of 1953—54 finally converted the cathedral to a functioning concert hall. This time, the builders added a suspended ceiling that isolated the hall from the dome; it remained in place as at end of 2007. Reduction of military personnel in 1960s made the concert hall redundant; in 1980 the cathedral reopened as a branch of the Central Museum of Navy.

The cathedral underwent extensive repairs and improvements, and was reconsecrated in April 2012. Repairs are completed in 2013, in time for the cathedral's centennial anniversary.

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