And he hoped to get that chance again. Now, he appears to have it.
The Kansas City Chiefs have agreed to acquire Smith from the 49ers in the first major acquisition since Andy Reid took over as the team's new coach in early January, a person with knowledge of the trade told The Associated Press on Wednesday.
The person spoke on condition of anonymity because the deal cannot become official until March 12, when the NFL's new business year begins. Another person familiar with the swap said the 49ers will get a second-round pick in April's draft, No. 34 overall, and a conditional pick in the 2014 draft.
After spending his first eight up-and-down years with the 49ers, Smith will get a welcome new start. The Chiefs will get the proven play-caller they hope can help turn things around under a new coach much the way Smith did under Jim Harbaugh in San Francisco.
"You never know when your opportunity's going to come," Smith said late in the season. "The good ones are ready when they do come."
The Chiefs have gone this route before, acquiring Joe Montana from the 49ers nearly 20 years ago, in April 1993, after he won four Super Bowls but gave way to Steve Young San Francisco's quarterback of the future.
Not so different from Smith's situation last season behind second-year QB Colin Kaepernick.
Moving Smith was hardly unexpected. He realized it once Kaepernick emerged as a capable starter over the season's final two months, and Smith all but said goodbye with his first pro team when he played briefly in the regular-season finale against Arizona to cheers of "Let's Go, Alex!" and "Alex! Alex!" from the Candlestick Park crowd.
With Smith now headed for Kansas City, Matt Cassel is likely headed out of town. And Reid will enter his first draft as Chiefs coach in April no longer needing to search for a quarterback.
The Chiefs' problems at quarterback are the single biggest reason they went 2-14 last season and secured the No. 1 pick in the draft for the first time in franchise history.
It's been a long-running problem for a franchise that has tried Steve Bono and Elvis Grbac (two more one-time 49ers), and more recently Damon Huard, Tyler Thigpen and Tyler Palko at quarterback. And then there's Cassel.
He was acquired by recently fired general manager Scott Pioli, and has two years left on a $63 million, six-year deal. He will likely be cut once Smith is acquired.
Cassel was benched last season in favor of Brady Quinn, who also is a free agent after going 1-7 as the starter.
If Smith can bring the steady form that defined his last two years, the Chiefs might be able to establish a much-needed consistency under center. They also found themselves a team-first player who led the 49ers through workouts during the 2011 lockout.
Under the three-year contract he signed last March, Smith is guaranteed $8.5 million in base salary for the 2013 season.
Smith thrived under 49ers coach and former NFL quarterback Harbaugh in one-plus season as the starter. Then, just like that, it all changed after he sustained a concussion.
Last week at the NFL combine, Harbaugh praised Smith and reiterated just how strong San Francisco was with Colin Kaepernick as the starter and someone with Smith's credentials at backup.
Yet everyone knew it was likely the 49ers would do their best to improve Smith's situation considering all he did for the franchise for nearly the past decade.
"Alex is really playing the best football of his career the last two years," Harbaugh said. "We think we got the best quarterback situation in the National Football League, feel strongly about that. Again, that'll be a process that plays out. Alex Smith continuing to be a 49er or if a trade occurs in the next weeks or months. Those are the two possibilities, most likely possibilities."
Smith acknowledged when he lost the job to Kaepernick back in November that he had done nothing wrong but get hurt. Not only had he completed 26 of his previous 28 passes 18 of 19 for 232 yards and three touchdowns without an interception and a 157.1 passer rating in a Monday Night Football win at Arizona on Oct. 29 Smith had just earned NFC Offensive Player of the Week honors after that victory in the desert.
He then sustained a concussion in the second quarter of a 24-24 tie against St. Louis on Nov. 11 saying later he threw a touchdown pass with blurry vision. Smith sat out the next game as Kaepernick dazzled in his debut as an NFL starter, beating the Bears handily at home on Monday Night Football.
After that, Harbaugh vowed to stick with the "hot hand," as he regularly put it, while complicating matters by still referring to Smith as a starter.
Smith's most poignant response to the situation was, "I feel like the only thing I did to lose my job was get a concussion."
Kaepernick led the 49ers to the NFC championship and a 34-31 loss to Baltimore in the Super Bowl in his second season. Now the 49ers are looking for his backup.
The 28-year-old Smith struggled for most of his career in San Francisco, plagued as much by coaching and constant coordinator changes as by his own indecisiveness. But when Harbaugh became coach in January 2011, Smith blossomed under the former QB's guidance. He was among the league leaders in passer rating (104.1) with a 70.2 completion percentage when he got hurt last season.
Fox Sports first reported the deal Wednesday.
AP Pro Football Writer Barry Wilner and AP Sports Writer Dave Skretta contributed to this story.