And while there are echoes of his departure from San Francisco in this situation, Smith says it's not exactly the same.
It helps that Smith is solidly the starter - as has been announced by the team, which also publicly tempered expectations for Mahomes (picked 10th overall in the draft).
Despite the fact that Smith led the Chiefs to just their second division title since 2004, it appears that the quarterback is on his way out in Kansas City.
"If any of us were the GMs, this is maybe the most important position in all of sports, and it would be insane not to be stockpiling talent", Smith said. "You'd be nuts not to, in my opinion". He knows this is year No. 13 for him in the NFL.
"But at the same time, that doesn't change my focus, right?"
Of course, the parallels to his time in San Francisco are natural. "He said he'll take me under his wing, and I really can't wait to start learning from him". But having had it happen to him before, he sees what's coming, eventually.
"They took a QB early, and that scenario and everything that comes with that is similar". Other than that, this is a completely different coaching staff, a completely different team.
Despite the regular-season success, however, Smith has been pigeonholed as a guy who can win you a lot of games but isn't the kind of difference maker to get you over the top and win a Super Bowl. "So all of those are very different".
That's one of the reasons he felt compelled to call Mahomes shortly after his selection and welcome him to Kansas City.
Indeed, Smith's seven-year tenure with the 49ers was riddled with changes - new offensive coordinators every year over four head coaches.
But if the Chiefs are ready to hand the keys over to Mahomes following his rookie season, they will have an opportunity to cut ties with Smith at a discount.
"I think (the Chiefs are) committed to me through this year", Smith said on Wednesday, via ESPN.
That's not the case with Smith though: The quarterback has been brutally honest while talking about his future with the Chiefs and working with Mahomes. There's a lot going on, you've got a thousand people (reaching out). I remember being there. "I just wanted to introduce myself and tell him to go enjoy it". We all have to, and those guys will tell you they're included in that. It can kind of being an overload. Sometimes it can be awkward, and it is. If you're not good enough and didn't get it done, you're not going to be around long. But you just embrace that and be real, and I think everybody kind of appreciates that. "You just kind of embrace that and be real. It's kind of the environment we have".
However, these comments are just another indication that Smith gets it. That's the nature of the position.