Construction began in 1857 on the site of the Stony Bar mining camp, when the chaos of the California Gold Rush demanded a more secure facility than San Quentin alone could provide. The prison officially opened in 1880 with cells measuring just a few feet wide, their solid boiler plate doors fitted with nothing but eye slots for light. Inmates spent most of their time in darkness. Air holes were not drilled into the cell doors until the 1940s. Folsom became the first prison in the United States to have electricity, an innovation that illuminated both its progressive ambitions and its harsh realities. The facility has served as the execution site for 93 condemned prisoners over its history.

Folsom's history reads like a compendium of desperate ingenuity. In 1920, three convicts hijacked a prison train and smashed it through the gates to freedom. In 1932, Dwight Abbott crafted a dummy so lifelike, using his own hair and a plaster of Paris face, that guards believed it was him sleeping until the next day's lockup. That same year, Carl Reese attempted an underwater escape using a diving suit fashioned from a football bladder and goggle lens. He drowned when his breathing tube proved too short. The most successful escape came in 1987, when Glen Stewart Godwin cut through fence wire, crawled 750 feet through a pitch-black storm drain, and floated down the American River on a raft, following painted arrows left by accomplices. Godwin was added to the FBI's Ten Most Wanted list in 1996 and remained there for nearly two decades before being removed in 2016. He remains a fugitive to this day.

Johnny Cash first wrote "Folsom Prison Blues" in 1955, a fictional account of an outlaw's incarceration inspired by a documentary film. The song became a country classic, but Cash felt he owed something to the real prisoners. His first Folsom concert came in 1966; the legendary 1968 recording session was captured in the cafeteria, where inmates crowded close enough to feel the music. The "Folsom Prison Blues" single from that album reached number one on the country chart for four weeks, and the album spent 122 weeks on the Billboard 200. Fifty years later, Los Tigres del Norte performed at Folsom to honor Cash's legacy, their concert filmed for a Netflix documentary.

Today, Folsom's Unit 1 holds the distinction of being the most populous cellblock in the United States, with capacity for nearly 1,200 inmates stacked across four five-tiered sections. The facility includes five housing units within its secure perimeter, two dining halls, and exercise yards where the violence of the 1970s and 1980s once made Folsom among America's most dangerous prisons. The Mexican Mafia, Black Guerrilla Family, and other prison gangs turned the yards into battlegrounds until the establishment of Secure Housing Units helped control the chaos. The prison's mailing address bears the name Represa, Spanish for "dam," a reference to the nearby Folsom Dam on the American River.

The granite walls of Folsom have appeared in dozens of films, from Inside the Walls of Folsom Prison to parts of Walk the Line, the Johnny Cash biopic. American Me, The Jericho Mile, and Another 48 Hrs. all filmed within its grounds. The 1995 film Heat references Folsom as home to its protagonist for seven years. The prison museum, housed in a former powerhouse, preserves artifacts from its violent past and displays memorabilia from the Cash concerts. Researchers from the El Dorado Hills Genealogical Society have worked since 2018 to identify the nameless graves in the prison cemetery, replacing numbered stones with the names of the dead.