On April 15, realizing that Fort Sumter's fall left the national capital of Washington, D.C. highly vulnerable to Confederate attack and occupation, President Lincoln called for 75,000 volunteers from around the Union to help defend it.

[15] On July 16, 1862, the U.S. Congress passed legislation authorizing the U.S. federal government to purchase land for national cemeteries for the purpose of burying military dead, and placed the U.S. Army Quartermaster General in charge of this program.

The government constructed rental houses that 1,100 to 3,000 freed slaves eventually occupied while farming 1,100 acres (450 ha) of the estate and receiving schooling and occupational training, both during the Civil War and after its end.

[18] On May 13, 1864, William Henry Christman was buried at Arlington Cemetery,[19] close to what is now the northeast gate in Section 27,[20] even though Meigs did not formally authorize establishment of burials until the following month, on June 15, 1864.

On March 3, 1883, Custis Lee sold it back to the U.S. government for $150,000 (equivalent to $4,161,818 in 2023) at a signing ceremony with then Secretary of War Robert Todd Lincoln.

[35] The property transfer, which involved 12 acres (4.9 ha) of NPS land, was intended to permit Metzler to start expanding the cemetery beyond its existing boundaries.

[37][47] The EA stated that the Interment Zone contained the oldest and largest tract of climax eastern hardwood forest in Arlington County.

[40] In addition, the legislation required the Secretary of the Interior to manage the remainder of Section 29 "in perpetuity to provide a natural setting and visual buffer for Arlington House, the Robert E. Lee Memorial.

"[40] In 2007, Metzler implemented the Millennium Project, a $35 million expansion plan to begin utilizing the Arlington woodland, Fort Myer, and Navy Annex land.

The Millennium Project expanded the cemetery's physical boundaries for the first time since the 1960s, and was the largest expansion of burial space at the site since the U.S. Civil War.

[50] The investigation also found that cemetery employees were burdened in their day-to-day work by "dysfunctional management, lack of established policy and procedures, and an overall unhealthy organizational climate.

In July 2008, The Washington Post reported that cemetery had imposed gradually increasing restrictions on media coverage of funerals beginning three years earlier, in 2005.

Hallinan had previously worked for the Office of Field Programs in the National Cemetery Administration, an agency of the United States Department of Veterans' Affairs.

[57] In September 2008, environmentalists expressed concerns that the agreement would result in the partial destruction of the 24-acre (9.7 ha) remnant of a historically important stand of native trees.

[58] On December 12, 2012, the United States Army Corps of Engineers asked for comments on a draft environmental assessment that described a further expansion of Arlington National Cemetery as part of the Millennium Project.

Although exact acreages were not specified and the plan depended upon the Commonwealth of Virginia's cooperation, the MOU if implemented would have created a more contiguous plot of land for the cemetery.

[71] On June 5, 2013, after reviewing 100 public comments that it had received on the revised environmental assessment, the Corps of Engineers released a final EA and a signed FONSI for the Millennium Project.

[81] In August 2015, the U.S. Army removed Lechner as superintendent of the cemetery after a performance review "called into question his ability to serve successfully as a senior leader".

[82] In December 2016, the National Defense Authorization Act for Fiscal Year 2017 (Public Law 114–328) authorized the Secretary of the Army to expand the cemetery by acquiring from Arlington County and the Commonwealth of Virginia by condemnation and other means properties near the cemetery that contain the Southgate Road, South Joyce Street and Washington Boulevard right-of-ways, including the Washington Boulevard-Columbia Pike interchange.

The Army would also acquire for the cemetery expansion about 7 acres (2.8 ha) of land located between Columbia Pike and Interstate 395 that the Commonwealth of Virginia then owned.

[84] In 2018, the US Army Corps of Engineers announced the expansion would allow for 40,000 to 60,000 additional burials and will incorporate the existing United States Air Force Memorial.

[85] The project covers 70 acres (28 ha) and by closing and relocating local roadways, allows the cemetery to utilize the former Navy annex property and remain contiguous.

[98] The United States Department of Veterans Affairs oversees the National Cemetery Administration's orders[99] for placement of inscriptions and faith emblems at no charge to the estate of the deceased, submitted with information provided by the next of kin[100] that is placed on upright marble headstones or columbarium niche covers.

[102] Prior to 2007, the United States Department of Veterans Affairs (VA) did not allow the use of the pentacle as an "emblem of belief" on tombstones in military cemeteries.

This policy was changed following an out-of-court settlement on April 23 following a series of lawsuits by the family of Patrick Stewart against the VA.[103][104][105] Between 1947 and 2001, privately purchased markers were permitted in the cemetery.

The remains of an unidentified American soldier from World War I were entombed on Armistice Day, November 11, 1921, later covered in 1931 by a more elaborate marble sarcophagus.

Transcribed on the back of the stone is the text of the John Gillespie Magee, Jr. poem High Flight, which was quoted by then President Ronald Reagan when he addressed the disaster.

[115] On June 25, 1925, President Calvin Coolidge approved a request to erect a Commonwealth Cross of Sacrifice with the names of all the citizens of the United States who died fighting in the Canadian forces during World War I.

[129] Two of the astronauts who were killed on January 27, 1967, by a flash fire inside the Apollo 1 command module, Gus Grissom and Roger Chaffee, are buried at the cemetery.

[130] British diplomat and Field Marshal Sir John Dill was buried at the cemetery when he died in Washington D.C. during World War II.