Carragher was representing England against World XI in the charity match, which raises money for underprivileged children across the world.
The former Liverpool defender started alongside John Terry at the back, and looked at home with the score 2-0 until late on in the first half.
DJ Locksmith clipped forward a ball looking for Bolt, and Carragher adjusted his body position to try to head clear the cross-field pass.
But the Sky Sports pundit mistimed his jump as the ball bounced over him into the path of the 100m world-record holder.
Bolt saw his opportunity and drilled a left-footed effort into the bottom right corner past David Seaman.
Watching on, Carragher’s long-term rival and former Manchester United captain Neville ended a short lay-off from Twitter to goad his colleague.
“I was off Twitter!” he wrote, insinuating Carragher’s mistake was too bad to ignore. “Embarrassing!”
World XI coach Piers Morgan obviously did not give the most riveting half-time team talk, as Carragher had time to reply while in the changing room.
“Read it all day, deceived by the bounce then a miss hit,” he responded, quoting Neville’s tweet.
“Nothing I could do T-bag.”
A number of fans took to the social media site to slam pundit Carragher.
One said: “We’d like to see Jamie Carragher analyse that one,” while another tweeted: “Waiting for @GNev2 analysis of Carragher’s defending #SoccerAid.”
Others were more simple in their appraisals of the goal, with one user tweeting: “Carragher AHAHAHAHAHAHAHAHAHAHAHA.”
“Looking forward to seeing full analysis of Jamie Carragher’s mistake there on a big touchscreen with 3/4 slow-mo replays,” joked another viewer.