Marathe replaces Gideon Yu in the role after the latter decided to step down, although he will remain as a co-owner of the team.
Al Guido, who worked closely with the 49ers as the senior vice president of Global Sales for Legends, will become the team's new chief operating officer, having helped them secure a move to their new stadium.
"As we move closer to the opening of Levi's Stadium, our organisation will continue to evolve and grow," 49ers CEO Jed York said in a statement.
"Gideon, Paraag and Al have been instrumental in making the new stadium a reality, and I couldn't be more excited about the future of our management team and the 49ers organisation.
"Paraag and Al have developed a tremendous working relationship and I am deeply confident in their leadership."
The 49ers will start playing at the Levi's Stadium next season after ending their 42-year stint at Candlestick Park.