He watched them rise to within a game of winning the 2011 Stanley Cup, and witnessed this season's catastrophic failure that culminated in the club's elimination from playoff contention with three games to go on the schedule.
Arguably the most popular player in franchise history, Linden returned to the fold Wednesday as the Canucks' new president of hockey operations.
And while most fans trumpeted the hire in what has been an otherwise miserable season, the team's former captain understands the honeymoon with a frustrated city could be a short one.
"I've kind of been like the backup quarterback the last few years, right?" Linden said with a smile at his introductory news conference at Rogers Arena. "Everyone loves the backup quarterback because he hasn't made any mistakes yet.
"I fully recognize what I'm getting into. I know that this market is passionate about the game, I know that there's an educated group of (reporters) that have opinions, but I wouldn't want it any other way."
Linden, who captained the Canucks for seven of his 19 NHL seasons, joined the team's front office just a day after president and general manager Mike Gillis was fired.
Gillis was the target of fan vitriol for a number of reasons during this lost campaign, including a spotty draft record, questionable trades and free-agent signings, and his handling of the Roberto Luongo-Cory Schneider affair that left the team without either goaltender.
Fans at a half-empty Rogers Arena chanted "Fire Gillis" in the dying minutes of Monday's demoralizing 3-0 loss to the Anaheim Ducks that sealed the Canucks' fate, and while team owner Francesco Aquilini wouldn't directly answer why Gillis was let go, it was clear he felt a fresh face was needed to reinvigorate a fanbase that had been spoiled with five straight playoff appearances.
"We came to within one game of winning the Stanley Cup," said Aquilini, who also thanked Gillis for his service. "It was time for a change. I'm disappointed, I think all the fans are disappointed. I'm big a fan. I'm a big fan and we need a new direction in the organization, a new voice.
"Trevor has exemplified great judgement in his career on the ice and off the ice and we have full confidence in him."
Linden played 15 seasons with the Canucks after being drafted second overall in 1988. He was named team captain at age 21 and led the team to the 1994 Stanley Cup final, where Vancouver lost in seven games to the New York Rangers.
A former president of the NHL Players' Association, Linden has no experience in an NHL team's front office. He said taking charge of the Canucks was something he couldn't pass up.
"Through my 20 years as a player, 15 years with the NHLPA and my more recent work in growing and leading a private business, I believe I'm ready for this challenge," said Linden, who is a partner in a Vancouver fitness club business. "I'm young, I'm passionate about this team, and I want to win, just like the Canuck fans do."
Linden had denied reports he would be taking over as president on Tuesday during an appearance on a Vancouver TV show. He said Wednesday he has apologized to the host of that show and that he couldn't confirm the reports at that time.
"It was an impossible situation to be in and out of respect for the process and certainly Mike (Gillis) and his family I had to do what I did," Linden said.
The 43-year-old Linden lives in Vancouver and said that while he enjoyed being away from hockey, the time was right to make a return.
"You don't spend 20 years in the National Hockey League and spend your whole life in hockey and not have it in your DNA," he said.
Linden said he met with the players and embattled head coach John Tortorella prior to being introduced and will begin a search for a general manager immediately with the hope of having someone in place in time for the draft in June.
"I like this core because there's good people there and they're character players and they deserve the right to be where they are," said Linden. "Having said that, at this juncture there needs to be a full evaluation of how we get better and what that looks like and there's many situations that play into that."
Tortorella, who like Gillis endured criticism this season for his defensive style, wouldn't speculate on his future now that Linden is at the helm.
"When someone comes into an organization, they have an organization view of how things should be done and Trevor will," said Tortorella. "I've said hello to him for 30 seconds. That may be my first and last conversation with him, or we may have other conversations. I don't know."
Aquilini also addressed a number of published reports in Vancouver that stated he had pressured Gillis into hiring Tortorella last off-season after the club fired Alain Vigneault.
"Mike hired Tortorella and I supported that decision," said Aquilini. "I have to take responsibility for that and that's why we have a change in direction today."
The deadline to renew season tickets, Aquilini said, was pushed back from Wednesday to April 17.
For their part, the Canucks' players said they felt responsible for Gillis' dismissal after the team failed to live up to expectations in 2013-'14.
"It's very disappointing when you are where we are with three games to go and it falls on us," said Canucks captain Henrik Sedin. "Whenever there's changes, as a player you take it up on yourself.
"It's been a failure and it's not fun. A lot of times someone's going to have to pay the price. Mike was the first one and we'll see what happens here."
At the NHL general managers meeting last month in Boca Raton, Fla., Gillis pointed to injuries and Tortorella's infamous locker-room outburst against the Calgary Flames as reasons for a disappointing mid-season swoon that saw the team win just four of 20 games.
Gillis was named NHL general manager of the year for the 2010-11 season and signed a contract extension after the 2011-12 campaign, but admitted in the radio interview that the Canucks' fall from grace put his job security in question.
Defenceman Kevin Bieksa said one day fans will look back and appreciate the work Gillis did for the club during his tenure that lasted just under six years.
"Mike did a lot for this organization in the short time that he was in charge, brought us to within a game of the Stanley Cup, a lot of division championships, two Presidents' Trophies," said Bieksa. "I think when the dust settles everybody will realize that Mike did a great job here.
"As a player you feel responsible for him being let go. We didn't get the job done this year and he had to pay the price."
The Canucks traded Linden to the New York Islanders during the 1997-98 season, and spent time in Washington and Montreal before being traded back to the Canucks early in the 2001-02 campaign.
His last season came in 2007-08, the last time the Canucks failed to make the playoffs. He played his final NHL game on April 5, 2008, and had his No. 16 retired by the Canucks later that year.
Sedin played with Linden early in his career and said he's right man to steer the team back into contention.
"I think you're going to see a calm influence, a guy that knows hockey," said Sedin. "He looks at the game of hockey the right way and he knows how to win. He knows how he wants to build the team and he's a great person."
Linden scored 375 goals and added 492 assists in 1,382 career NHL games. He served as NHLPA president for eight years, a span that included the lockout that cancelled 2005-06 season.
"Part of the reason you love the game as a player is because you love the thrill of victory and the agony of defeat, and it becomes addictive," said Linden. "Part of the reason about being back in this chair today is about the opportunity to win, the chance to win, the chance to do something special here in Vancouver.
"For me this is the right step at the right time and it's a good fit and I'm excited to get started."