Beckwith was born to Jessie Harlan Lincoln and Warren Wallace Beckwith on August 22, 1898, in Mount Pleasant, Iowa. She got the nickname "Peggy" from her grandfather Robert Todd Lincoln, who described her hair as "flying in the sun" when he wrote to his Aunt Emile Todd Helm. People who were close to her called her "Peggy." Raised with her brother at Hildene, the family estate in Vermont, she later grew up in Washington, D.C., and was said to have become "a squat, fair-haired, blue-eyed, chain smoker who golfed and dabbled in oil painting and sculpture." Beckwith attended Miss Madeira's school, a private prep school, but she did not go on to college afterwards. Prior to World War I, she was a representative on the committee on public information in Cuba. In 1918, she returned to the family farm to fill positions left by men who had gone to war. Beckwith took an agricultural course at Cornell, and wanted to organize young women to work the farm. Beckwith was interested in aviation. Her first time flying was to ask for a ride in a plane at the Curtiss airport in Baltimore in 1930 and afterwards "she announced without any further formalities that she would like to learn to fly by herself." She earned her private pilot's license by 1931. In the 1930s, she built a private landing strip at Hildene, and purchased a number of airplanes. One of them was a three-seat sports plane. She also owned a Cutliss Gypsy Moth and a Traveler. During this time she was living at Hildene with her grandmother, Mary Harlan Lincoln. By 1938, Beckwith was operating a 1,000 acre dairy farm at Hildene. She had inherited this property following the death of her grandmother, Mary Harlan Lincoln in 1938.
Later life
Beckwith later in life became an eccentric recluse at Hildene. She never married or had children. Beckwith ran the estate "as a farm" and dabbled in art and sculpture. Despite her desire to eschew publicity, she was well-known by the local farm community. She was known to conduct errands in the town around Hildene "dressed in blue jeans overalls, with a shirt and a man's cap." Beckwith christened the submarine, the Abraham Lincoln, on May 14, 1960. She died on July 10, 1975 at around 2:15 a.m. at Rutland Hospital in Rutland, Vermont. She had requested that her ashes be spread over her estate; this request was granted and there was no funeral or memorial service held. Upon her death, her brother Robert Todd Lincoln Beckwith became the last living descendant of Abraham Lincoln.