Oakland Roots

The club was formed in July 2018, and would be known as Oakland Roots Sports Club. The club originally was slated to play in the NPSL Founders Cup, but the club ultimately withdrew and instead joined the National Independent Soccer Association, a Division III sanctioned United States Soccer Federation professional league.

Oakland Roots began by signing three Oakland-raised players in the spring of 2019: Devante Dubose, Julio Cervantes and Yohannes Harish. This was followed by the signing of several higher-profile players as the club built out its inaugural rosters. Those players included former San Jose native and MLS player Benji Joya, former Honduran World Cup veteran and San Jose Earthquake Victor Bernardez, and former first-round MLS draft pick Jack McInerney.

The club announced Bay Area native and former MLS player and Colorado Rapids technical director Paul Bravo as its first head coach on May 9, 2019.

National Independent Soccer Association

The club opened the inaugural 2019–20 NISA season as the league's first game, at home in front of a sold-out crowd of more than 4,500. McInerney would score a first-half perfect hat-trick in a match that would eventually end up in a 3–3 draw.

Oakland Roots played eight games in their inaugural season: six in NISA and two friendlies against Mexican clubs FC Juarez and Atlético Zacatepec. The club picked up their first win at home against Atlético Zacatepec by a score of 2–0.

Oakland Roots sold out all four of their home games in the 2019 fall season averaging 4,927 fans, including a record 5,723 in their final home game, a 1–1 draw vs Los Angeles Force.

On October 31, 2019, Oakland Roots and Bravo mutually agreed to part ways. On December 3, 2019, Oakland Roots announced Jordan Ferrell as the club's new head coach.

The Roots opened their second season at home once again in front of a sold-out crowd of 5,603. The match against Chattanooga FC would end in a 1–1 draw when McInerney scored in the 93rd minute of the match after the Roots were forced to play a man down from a first-half red card. The Roots followed this up by winning their first-ever NISA league match the following weekend vs Michigan Stars FC 2–1.

On April 27, 2020, following an extended stoppage of play due to the COVID-19 pandemic, NISA announced the cancellation of the 2020 spring season.

In the abridged 2020 fall regular season, Oakland finished first in the three team Western Conference, with Matthew Fondy leading the team with two goals. The Roots finished atop its group in the NISA Fall Championship, and beat Chattanooga FC in the national semifinal, before falling to Detroit City FC, 2–1, in the final.

USL Championship

On September 15, 2020, the team announced they would be moving from the third-division NISA to the second-division USL Championship.

Initially, in 2017, the USL approved a bid from real estate developer Mark Hall to bring a soccer team to Concord, California, instead of Oakland. The team, called USL East Bay, planned to play in a 15,000+ seat soccer-specific stadium complex before the development idea was scrapped in May 2020. The team's territorial rights were later sold to the Roots.

In November 2020, Oakland Roots announced the signing of Oakland born, Richmond, California raised midfielder Saalih Muhammad via a transfer from New Mexico United as the club's first USL Championship player. This was followed by the early December signings of Oakland raised Max Ornstil and re-signings of Yohannes Harish and Tarn Weir, as well as many others.

In April 2021, Marshawn Lynch joined the Roots ownership group.

Oakland Roots picked up their first USL Championship win on May 23 at LA Galaxy II when striker Jeremy Bokila scored in stoppage time to give Oakland the 3–2 win. The team was set to kick off the USL Championship home season on June 19 against Sacramento Republic FC, but the match was called off due to field issues. This was then followed by multiple games being called off due to USL health and safety protocols during the COVID-19 Pandemic.

The team went on to play multiple games at Las Positas College before finishing the season back home at Laney. The club had just one win through their first 13 games. The club placed dead last in the USL Power Rankings in August.

The team initiated a massive turnaround with a 2-1 victory at Merritt College, propelled by goals from Ornstil and Harish. Following this triumph, Oakland proceeded to secure 34 points in 19 games, ultimately earning the final Pacific Division playoff position on the last day of the season after a 1-0 win against Sporting Kansas City II.

Oakland upset the Mountain Division Champions El Paso Locomotive in the first round of the playoffs, breaking a 470-day home unbeaten run by the Texas side. The Roots’ playoff run came to an end the following weekend when the team lost 6–5 on penalties against Orange County SC after 120 minutes of scoreless action.

On December 21, 2021, the Roots announced they were leasing the former Oakland Raiders practice facility in Alameda, California as their training facility.

On December 30, 2021, the Roots announced Juan Guerra as the club's fourth head coach.

On October 23, 2022, the Roots upset San Diego Loyal 3–0 in the first round of the playoffs. This punched their ticket to play San Antonio, where they lost 3–0.

On September 18, 2023, the team announced that Green Day singer Billie Joe Armstrong joined the ownership group for the Roots. Additionally, the team opened for community investment and ownership that month.

On October 26, 2023, the team announced that NBA Head Coach Jason Kidd joined the ownership group for the Roots.