Marotta joined Juve in 2010 and presided over a glorious period for the club, which included seven consecutive Serie A titles before stepping down at the end of September.
The 61-year-old had been heavily linked with the presidency of the Italian Football Federation (FIGC) towards the end of his tenure, but he strongly denied that and claims of talks with Inter surfaced soon after.
Marotta's installation will surely come with great expectations given Juve's success under his guidance, coupled with Inter's underwhelming showings in recent years.
The Nerazzurri have not won the title since 2009-10, but they will hope Marotta's arrival is the first step on the road to domestic success once again, with their new chief well aware of the requirements needed to win the Scudetto.
Speaking in a video posted on Inter's official Twitter account, Marotta said; "From today [Thursday] I'm part of the great Inter.
"It's a source of great pride for me. I'll hold the important position of CEO of the sporting area.
"This is an important experience in my professional life, full of great responsibility. That doesn't scare me, though. You start a new path and you have to be a winner."
Marotta's official title will be Chief Executive Officer Sport, with Alessandro Antonello working in the same role but focusing on the club's corporate activities.
The pair join the club with Luciano Spalletti's men a respectable third in the table, but they are already 14 points adrift of pacesetters Juve.
"This is an important change for the club in line with our objective of becoming a winning football club and a successful company," said president Steven Zhang.
"As Inter, we want to win, entertain, inspire and connect people through football. Beppe is one of the best executives in the football industry and will help us to achieve our goals.
"Outside of the pitch Alessandro will ensure the enhancement of our off-pitch performance, the successful completion of the club's strategic projects, and the promotion of our values inside the organisation."