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Hunter graduated West Point in 1822, ranked 24th in his class. He served minor positions on the Northwest frontier before the war. On May 14, 1861, he was made colonel of the 3rd U.S. Cavalry. Only 3 days later, he was named brigadier general in charge of the 2nd Division of Brig. Gen. Irvin McDowell's army, and on Aug. 13 received a promotion to major general. When the war commenced, he was seriously wounded at First Bull Run.
Hunter was later sent to Missouri and put in charge of a division under Maj. Gen. John C. Fremont, whom he relieved as commander of the Western Department. In 1862 he took over the Department of the South and subsequently captured Fort Pulaski, Ga., demanding its surrender. On May 9 he abolished slavery in his department of the army, an action repudiated by Pres. Abraham Lincoln on the grounds that Hunter had overstepped his bounds. Hunter then raised a black regiment, the 1st South Carolina, which was approved by Congress.
Hunter was defeated at Secessionville on June 16, 1862, in an effort to capture Charleston. Afterward, he temporarily suspended his military duty. When Maj. Gen. Franz Sigel was deterred in the Shenandoah Valley in May 1864, Hunter took over the Department of West Virginia in the valley region. He severed Southern supply, communication, and railroad lines as he moved throughout the valley. He found victory at the Battle of Piedmont, but at Lynchburg, encountered forces under Lt. Gen. Jubal Early, who caused Hunter to withdraw into West Virginia. The move left the valley open for Early's Washington Raid, leaving Hunter to receive much criticism for his retreat. After meeting with Lt. Gen. U.S. Grant and Maj. Gen. Philip Sheridan, he chose to resign his command Aug. 8, 1864, allowing Sheridan to effectively rid the Shenandoah Valley of Confederate forces. Known for the numerous defeats he suffered, Hunter is not considered among the more adept Union military officers.
Following Lincoln's assassination, Hunter served as president of the committee that tried the conspirators. Following the war, he received brevets to brigadier and major general in the Regular Army. He lived in Washington D.C. until his death on February 2, 1866.
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