The four-time Pro Bowl cornerback visited the team on Saturday and quickly agreed to contract terms with the team. The deal is worth $39.15 million with a $5 million signing bonus, according to the NFL Network.
The two parties came to an agreement one day after Sherman was officially released by the Seattle Seahawks with a failed physical designation. He reportedly had dinner with 49ers coach Kyle Shanahan on Friday night, per The Athletic.
"Richard is one of the premier competitors Kyle and I have ever encountered," 49ers general manager John Lynch said in a statement. "We look forward to him sharing his wealth of experience and his passion for the game of football with our team. Richard has long been looked at as the prototypical corner in our scheme and the opportunity to have him mentor our players was one we needed to attack. Most importantly, we are excited to have a championship caliber corner on the field for the 49ers."
The 49ers were interested in making certain Sherman is healing from his injuries, ESPN's Adam Schefter previously reported, and apparently are convinced that he will recover.
NFL Network reported Saturday that Sherman had scheduled a visit with the Detroit Lions, who were also interested.
Sherman, who will turn 30 on March 30, is coming off a season-ending Achilles tear, as well as a surgical procedure on his other Achilles.
"I want to go to a contender," Sherman told KIRO-AM in Seattle on Friday. "I play at a high level. I've always been a guy that can work well with others and continue to elevate if my teammates elevate and elevate others.
"Would I go to a young secondary that is like we were when we were younger and help them grow and help them advance? Sure, if the number looks right and the situation is comfortable for me and my family."
Sherman attended Stanford but spent the last seven seasons in the Pacific Northwest. He had noted that the Seahawks informed of him that they were still open to re-signing him but that won't happen now.
He had one season remaining on a four-year, $56 million extension he signed in 2014 after the Seahawks won Super Bowl XLVIII.
Sherman has a league-best 32 interceptions since entering the NFL in 2011 as a fifth-round draft pick.
He was also the vocal leader of a defense that led Seattle to back-to-back Super Bowl appearances.
Sherman played only nine games in 2017 before sustaining a season-ending ruptured Achilles tendon.
During his seven years in the Northwest, a handful of incidents involving Sherman and the 49ers incited bad blood between the two teams.
Some of those occurred on the field, including a game-saving interception in the 2014 NFC Championship Game. Others, like Sherman ripping then-49ers wide receiver Michael Crabtree as "sorry" and "mediocre," took place, off the field.
The brash Sherman also didn't mince words when it came to former 49ers coach Jim Harbaugh, his coach at Stanford, calling him a bully.
But all seemed forgiven as Twitter reaction from Sherman's former enemies was quick.
Offensive tackle Joe Staley: "As much as I disliked playing against him for years, I know I will love being teammates with him going forward. Pumped to have @RSherman_25 as a teammate!!"
Fullback Kyle Juszcyck: "I take back anything disrespectful I might have said to you in our games before @RSherman_25 Welcome to the squad!!"
Fellow cornerback Ahkello Witherspoon: "@RSherman_25 welcome big dawg!! Let's get this ...."
Safety Dexter McCoil: "It's lit ... We not playing ... I can't wait to hit the field."