The ship began life under the Imperial flag. She was one of eight Fidonisy-class destroyers built for the Imperial Russian Navy during the First World War, launched in 1916 under the name Kaliakria. Even her armament reflected the moment: unhappy with the anti-aircraft guns originally planned, the navy swapped in a pair of Hotchkiss guns while she was still under construction in 1917, the year the empire that ordered her fell. In 1926 she was renamed Dzerzhinsky, after the founder of the Soviet secret police, and carried that name into a second war a generation later. Fast for her size, with four single 102-millimeter guns and banks of torpedo tubes, she was a relic of one era pressed into the service of the next.

When Germany invaded in June 1941, Dzerzhinsky was stationed at Batumi and immediately went to work, laying 240 mines off the naval base in four night sorties. Then came Odessa. With larger ships held back after heavy losses, the aging destroyers carried the burden of supporting the city's defenders. Dzerzhinsky ran ammunition in and wounded out, bombarding Axis positions at Dofinovka and Fontanka, expending hundreds of shells at a stretch. The work was punishing and improvised: a turret elevator failed and had to be reloaded by hand, artillery fragments damaged a gun and her torpedo tubes, and more than once she slipped out of the burning port under her own smokescreen, nearly out of fuel and with no drinking water left aboard.

By May 1942 the focus had shifted to besieged Sevastopol. Loaded with reinforcements at Novorossiysk, Dzerzhinsky approached the harbor channel on the foggy night of 13-14 May and waited for the visibility she needed to thread a Soviet minefield. Late that morning, with commanders fearing the ships had drifted too close to the mines, she was ordered to find the minesweeper marking the cleared lane. She turned toward it without deploying her paravanes. Before she reached it, at 12:20, she struck a mine and went down fast. Of 170 crew and 125 passengers, only 27 survived, her captain among them. Struck from the navy that summer, she lay unfound until 2006, when a Ukrainian-American expedition located her wreck on the Black Sea floor.