Okhotsk was the first Russian settlement on the Pacific Coast. It was established as a wintering camp in 1643 by the Cossacks under Semyon Shelkovnikov. The fort of Kosoi Ostrozhok was constructed in 1649. In 1718 Kozma Sokolov built the first vessel in Okhotsk and embarked upon a voyage to Kamchatka. This route became so popular with Russian navigators that by 1731 Okhotsk had been firmly established as the foremost Russian seaport on the Pacific.
At various points in its history, Okhotsk was a centre for the Russian-American Fishing and Fur-Trading activities. It is known for being the headquarters for the explorer Vitus Bering, who sailed from here for two extraordinary expeditions, discovering the Bering Strait on one and Alaska on the other. The Portuguese Jew Anton de Vieira was the town's governor at that time.
The growth of Petropavlovsk-Kamchatsky dislodged Okhotsk from its leading commercial position in the early 19th century, although it remained important as the base of the Siberian military flotilla, a predecessor of the Russian Pacific Fleet. In 1812 the town was moved to a new site across the Okhota River. It was of some military importance during the Russian Civil War, when the White army generals Vasily Rakitin and Anatoly Pepelyayev used it as their place of arms in the Far East.