Ruti Aga was born on 16 January 1994 in Ethiopia. She began her competitive career as a junior track runner, winning silver in the 5,000 meters at the 2012 World Junior Championships in Barcelona and gold at the 2013 African Junior Athletics Championships. She ran her first marathon as a pacemaker at the 2016 Osaka Marathon and placed third at the Berlin Marathon that autumn.
She placed second at three consecutive World Marathon Majors: Berlin 2017, Tokyo 2018, and Berlin 2018, where she finished in 2:18:34, a time that ranked her sixth in history at the time. She broke through for her first major win at the 2019 Tokyo Marathon, covering the course in 2:20:40 to win by 21 seconds. She was the only woman ever to have run sub-2:20 without previously winning a marathon before that victory.
In October 2023, she set her personal best of 2:18:09 at the Dongying Marathon in China, then equalled that mark at the 2024 Dubai Marathon. Her half marathon best of 1:06:39, set at the 2018 Houston Half Marathon, was the second-fastest ever recorded on U.S. soil at the time.