Johnson-Thompson, a heptathlon specialist but who has concentrated mainly on the long jump this indoor season, recorded a personal best of 6.81m to take silver in Sopot.
She leapt the distance with her second attempt on the runway at the Ergo Arena and initially took the lead however Eloyse Lesueur of France would eventually overthrow her.
She jumped 6.85m with her fourth attempt while Johnson-Thompson admitted that silver was more than she could have imagined returning to the UK with.
"It's hard to believe isn't it? I've done World Junior Championships before and now I've won my first senior international medal," said Johnson-Thompson, who finished an impressive fifth at last year's outdoor World Championships.
"Everybody knows I'm a heptathlete and I will be going back to the heptathlon. I just really can't believe it. I came here with no expectations at all.
"I thought if everyone has a bad day or somebody doesn't turn then I might be able to sneak a medal. It was unbelievable that I was winning but I'm so happy with a silver medal."
After an impressive 60m gold for Richard Kilty on Saturday along with Tiffany Porter's 60m hurdles bronze, Johnson-Thompson's silver was one of four British medals claimed on the final day.
The British men's 4x400m relay quartet took silver and the women's 4x400m team bronze while Andrew Osagie climbed the podium at a second successive World Indoor Championships.
He took 800m bronze in Istanbul two years ago but needed Marcin Lewandowski's disqualification to repeat the trick; Osagie admitting to a hollow victory in Sopot.
"There was a lot of battling for the front in the first lap and I tried to stay out of it and pick my time to move and unfortunately got stuck," he said.
"I was in fifth place with less than 100m to go and I saw him step off the track and athletes instinct was that's not allowed.
"Tactically I didn't run that well in the final and apart from the medal, which was from the DQ of somebody else, I haven't got a lot of positives to take away from the final.
"It's very bittersweet because I get on with Marcin very well on and off the track so it's going to be a bit awkward from now. I'm very happy to add to the medal tally for GB & NI though."
� Sportsbeat 2014
World Indoor Championships
Fraser-Pryce triumphs, US men set relay record
09/03/2014 AT 20:57