Later life
Following his term as governor, Holton served one year in the Nixon Administration as the Assistant Secretary of State for Congressional Relations. After leaving Washington, he practiced law as a shareholder at McCandlish Holton, P.C.
Holton later unsuccessfully sought the Republican nomination for the United States Senate in 1978, finishing third in a race against Richard D. Obenshain, John Warner, and Nathan H. Miller. Warner subsequently became the nominee after Obenshain's death in a plane crash.
Under Gerald Baliles (1986–1990), he served as interim president of the Center for Innovative Technology in Northern Virginia, where he guided it through managerial difficulties.
After his retirement, Holton supported moderate Republicans, including John Warner. As the Virginia Republican Party became more conservative, however, he found himself more in line with the state Democratic Party and endorsed several Democrats for statewide office, including his son-in-law, Governor Tim Kaine. Holton endorsed Barack Obama in the 2008 presidential election.
The Holtons had four children: Tayloe, Anne, Woody, and Dwight. Anne is married to U.S. Senator and former Virginia Governor Tim Kaine, the nominee of the Democratic Party for Vice President of the United States in 2016. She was the first First Lady of Virginia to live in Virginia's Executive Mansion both as a child and as a First Lady. In January 2014, Anne Holton was named Virginia Secretary of Education. Woody Holton (Abner Linwood Holton III) has published three books, including Unruly Americans and the Origins of the Constitution (2007), a finalist for the National Book Award, and Forced Founders: Indians, Debtors, Slaves and the Making of the American Revolution in Virginia (1999). His third book, a biography of Abigail Adams, won the Bancroft Prize in 2010. Dwight Holton served as acting U.S. Attorney for Oregon from 2010 to 2011. He later lost to Ellen Rosenblum in the May 2012 primary in the race for Oregon Attorney General.
In 1999, Linwood Holton Elementary School, in Richmond, Virginia, was named in his honor.
In November 2005, Holton underwent surgery for bladder cancer. In 2006, Holton, his wife Jinks, daughter Anne and son-in-law Tim Kaine opposed a proposed constitutional ban on same-sex marriage in Virginia.
The University of Virginia Press published his memoir, Opportunity Time, in March 2008. He was a long-time member of the Governing Council of the University of Virginia's Miller Center of Public Affairs.
In 2017, the City of Roanoke hosted Holton for the dedication of a plaza named in his honor.
On the day of Ralph Northam's inauguration in January 2018, Holton sat front and center for a photograph with Northam and nine other former governors who had followed Holton, including Bob McDonnell, Jim Gilmore, Tim Kaine, Terry McAuliffe, George Allen, Mark Warner, L. Douglas Wilder, Chuck Robb, and Gerald Baliles.