Togiak is the successor village of two earlier Inuit villages, Togiagamute (Togiagamiut) & Togiak Station (also known as Togiak or Owens). The prior two villages were on the eastern side of Togiak Bay. By the early 20th century, heavy winter snowfalls made wood gathering difficult, so residents began to relocate to the west side of the bay to the new village of Togiak, which first appeared on the 1920 census. The earlier village of Togiagamute is now within the adjacent Twin Hills CDP, and the old site is still occupied. Togiak Station, about 7 miles south of the former Togiagamute, is now a ghost town.

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The Togiak area became a draw for natives in the vicinity after the devastating influenza pandemic of 1918–19, which had almost wiped out many villages. Togiak was flooded in 1964, which prompted some residents to relocate and establish the new community of Twin Hills, northeast of the original village of Togiagamute on the upper east side of the bay.