Facing the possibility of an embarrassing draw against the soccer minnows, Johnson headed home an Alan Gordon cross in the 90th minute to keep the Americans' destiny in their own hands ahead of the final stage match against Guatemala on Tuesday.
The U.S. need to finish in the top two of their CONCACAF group to advance to the final qualifying round in the Central and North America and the Caribbean regions.
They had been locked in a three-way tie with Guatemala and Jamaica in the group prior to the match and a win in their last match on Tuesday will guarantee a place in the final stage of qualifying for the 2014 World Cup finals in Brazil.
After a lean time in Europe over the last few seasons, Johnson signed with Major League Soccer's Seattle Sounders this season and found his form, prompting Klinsmann to add him to the squad for the final two games of qualifying.
Looking for an aerial advantage it proved a masterstroke as Johnson opened the scoring in St John's with a header from a Graham Zusi cross in the 20th minute.
Antigua tempered American celebrations just five minutes later when Peter Byers beat his man for pace and crossed low for Dexter Blackstock to equalise from close range.
With time ticking away Johnson produced the match-winner to validate Klinsmann's faith.
"All I can say is we talk about dreams and making dreams a reality and it's good to be back," Johnson said. "The coach had a tonne of confidence in me and the players had confidence in me which makes it really easy to come into the system."
It wasn't all good news for the U.S. with Jermaine Jones picking up a yellow card that will keep him out of the match with Guatemala.