Eagle River was a boom town of the copper mining era in the Keweenaw. Copper was discovered in 1845 at the Cliff Range nearby, the so-called "Cliff Lode". The land of the Eagle River community had been leased by the Keweenaw Copper Company in 1843. It was later platted by the Phoenix Company and sold as individual lots. The first postmaster was named on October 24, 1845. It was part of Houghton County until Keweenaw County was organized in 1861. The profitability of the area's copper mines had begun to decline sharply by around 1870.
The Eagle River Timber Bridge is a wooden arch bridge that carries highway M-26 over the Eagle River. It opened in 1990 as a replacement for the historic Lake Shore Drive Bridge that runs parallel to it.
Eagle River is home to the Holy Transfiguration Skete, a Byzantine Catholic monastery and community, which is known for producing jams and other foodstuffs from berries collected in the nearby forests. Holy Transfiguration is one of only a few Byzantine Catholic monasteries in the United States.
The community of Eagle River was listed as a newly-organized census-designated place for the 2010 census, meaning it now has officially defined boundaries and population statistics for the first time.