A strong opponent of slavery Hunter corresponded with Abraham Lincoln on the subject and was invited to Washington in January, 1861. On the outbreak of the American Civil War he joined the Union Army and became colonel of the 3rd United States Cavalry and was severely wounded at Bull Run (July, 1861). After he recovered from his wounds he replaced Major General John C. Fremont as commander of the Western Department.
In March, 1862, Hunter was appointed Commander of the Department of the South. After the successful campaign at Fort Pulaski he began enlisting black soldiers in the occupied districts of South Carolina. He was ordered to disband the 1st South Carolina (African Descent) but eventually got approval from Congress for his action.
Hunter also issued a statement that: "The persons in these three States - Georgia, Florida and South Carolina - heretofore held as slaves, are therefore declared forever free." Abraham Lincoln quickly ordered Hunter to retract his proclamation as he still feared that this action would force slave-owners in border states to join the Confederates. President Jefferson Davis and the he leaders of the Confederate Army were furious when they heard of Hunter's actions and orders were given that he was a "felon to be executed if captured."
Horace Greeley, editor of the New York Tribune, wrote an open letter to Abraham Lincoln defending Hunter and criticizing the president for failing to make slavery the dominant issue of the war and compromising moral principles for political motives. Lincoln famously replied: "My paramount object in this struggle is to save the Union, and is not either to save or destroy slavery. If I could save the Union without freeing any slave, I would do it; and if I could save it by freeing all the slaves, I would do it."
Hunter served on the court-martial of Fitz-John Porter and the committee that looked into the loss of Harpers Ferry. He also served on several other boards and commissions before replacing Major General Franz Sigel during his Shenandoah Valley campaign in May, 1864. Hunter fared little better than Sigel and was defeated by Major General Jubal Early at Lynchburg in June. He now resigned his commission and was replaced by Philip Sheridan.
Hunter accompanied the body of Abraham Lincoln to Springfield and afterwards was invited by President Andrew Johnson to be a member of the nine-man military commission to try the conspirators to assassinate President Lincoln. It was argued by Edwin M. Stanton, the Secretary of War, that the men should be tried by a military court as Lincoln had been Commander in Chief of the army. Several members of the cabinet, including Gideon Welles (Secretary of the Navy), Edward Bates (Attorney General), Orville H. Browning (Secretary of the Interior), and Henry McCulloch (Secretary of the Treasury), disapproved, preferring a civil trial. However, James Speed, the Attorney General, agreed with Stanton and therefore the defendants did not enjoy the advantages of a jury trial.
The trial began on 10th May, 1865. As well as Hunter the military commission included leading generals such as Lewis Wallace, Robert Foster, August Kautz, Thomas Harris and Alvin Howe. The Attorney General, James Speed, selected Joseph Holt and John Bingham as the government's chief prosecutors.
Mary Surratt, Lewis Paine, George Atzerodt, David Herold, Samuel Mudd, Michael O'Laughlin, Edman Spangler and Samuel Arnold were all charged with conspiring to murder Lincoln. During the trial Holt attempted to persuade the military commission that Jefferson Davis and the Confederate government had been involved in conspiracy.
Joseph Holt attempted to obscure the fact that there were two plots: the first to kidnap and the second to assassinate. It was important for the prosecution not to reveal the existence of a diary taken from the body of John Wilkes Booth. The diary made it clear that the assassination plan dated from 14th April. The defence surprisingly did not call for Booth's diary to be produced in court.
On 29th June, 1865 Mary Surratt, Lewis Paine, George Atzerodt, David Herold, Samuel Mudd, Michael O'Laughlin, Edman Spangler and Samuel Arnold were found guilty of being involved in the conspiracy to murder Abraham Lincoln. Surratt, Paine, Atzerodt and Herold were hanged at Washington Penitentiary on 7th July, 1865. Surratt, who was expected to be reprieved, was the first woman in American history to be executed.
The decision to hold a military court received further criticism when John Surratt, who faced a civil trial in 1867, was not convicted by the jury. Michael O'Laughlin died in prison but Samuel Mudd, Edman Spangler and Samuel Arnold were all pardoned by President Andrew Johnson in 1869.
David Hunter died in Washington on 2nd February, 1886.