The Pigeon River flows in an easterly direction out of the Boundary Waters Canoe Area Wilderness for 31.2 miles (50.2 km) until it drains into Lake Superior.

Up to the 19th century, the river was a primary water route for fur traders, and even earlier, for Native Americans, leading to the Lake of the Woods and thence to western Canada and Hudson Bay.

The Montreal-based North West Company had a post at the community of Grand Portage on the shore of Lake Superior until 1801 when difficulties with the U.S. government following the adoption of the Jay Treaty obliged it to relocate to the Kaministiquia River in British territory.

[4] An "outlaw" bridge across the river was built by residents of Thunder Bay, Ontario, and opened on August 18, 1917, to permit access to Minnesota.

The river's English name is a translation of the 18th century French name Rivière aux Tourtres or Tourtes derived after the passenger pigeon which was once prolific in this region.