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Petropavlovsk was founded in 1741 by Vitus Bering, the Danish-born Russian captain who discovered the straits that bear his name. The slowly developing town was named for Bering's two ships, the Svyatoy Pyotr (St Peter) and Svyatoy Pavel (St Paul); 'Kamchatsky' was added to distinguish it from all the other Petropavlovsks. It became the tsars' major Pacific sea port and was used as the base for explorations that turned up the Aleutian Islands and Alaska.

There were some unlikely visitors in 1779, when Captain Clerke, sailing under the British flag, entered the Petropavlovsk harbour in command of Captain James Cook's former ships (Cook had lost them, and his life, two years before in Hawaii). Clerke intended to travel the Arctic, but shortly after setting out was stricken with consumption and died. In August 1854 more British (with the French in tow) sailed into Avacha Bay with more permanent goals in mind. This seaborne Crimean War invasion was successfully and unexpectedly repulsed by the small Petropavlovsk garrison.

During the Soviet era the town became a sizable Pacific Fleet submarine base, but its present prosperity is owed completely to the fishing industry. Rusting Petropavlovsk trawlers bring in a million tonnes of fish a year, of which nearly half is sold to Japan.