Australia took another major step towards next year's tournament in North America with a gutsy 2-0 win over China on Tuesday night.
First-half efforts from the in-form Jackson Irvine and Nishan Velupillay at a near-sold out 80,000-seat Olympic Sports Centre Stadium in Hangzhou on Tuesday continued Popovic's unbeaten start to life as national-team boss.
Not since Terry Venables in the 1990s has a Socceroos manager avoided defeat through their first six games.
But that will mean nothing if Popovic does not successfully navigate a pivotal June window.
Australia take on Japan in Perth on June 5 in the first game of the window while Saudi Arabia face a short away trip to neighbours Bahrain before hosting the Socceroos on June 10 in a potential winner-takes-all encounter.
The Socceroos last beat Japan in Melbourne in 2009, but can take heart from October's 1-1 draw in Saitama.
The win over China has meant Australia, (13 points, +7 goal difference) retains the second automatic qualification spot in Group C.
But Saudi Arabia (10 points, -2 goal difference) are within touching distance after they held the already-qualified Japanese to a 0-0 draw in Saitama on Tuesday.
Goal difference decides which side will finish higher with the third and fourth-placed teams facing another round of qualifying.
In the group's other match, Indonesia beat Bahrain 1-0 in Jakarta to leapfrog their opponents into fourth with nine points.
That result meant Australia are assured of at least reaching the fourth qualifying round, but automatic qualification, last achieved in 2013 for the Brazil World Cup, remains the goal.
"Now the challenge is a great one," Popovic said.
"You've got Japan and Saudi … can we improve once more in June against the best in Asia?
"We were in front when we started this window … we did our part. We got six points. We extended our lead to three (points).
"We're in a good position because it's in our hands.
"But we have to get the job done (these are) two wonderful games coming up, first Japan in Perth, it will be a special match."
On Tuesday night, China - needing a win to revitalise their own hopes of automatic qualification - were bordering on passive for the opening 45 minutes.
Melbourne Victory's Ryan Teague, who is coincidentally also eligible for China, was handed a starting debut and did not look out of place at the base of the Australian midfield.
"It was a great way to start … he's a very level-headed young man and he gave us some good balance," Popovic said.
Australia broke the deadlock after 16 minutes when Lewis Miller squared to Irvine on the edge of the China box.
Both Huang Zhengyu and Li Lei were unable to dispossess the dogged and determined St Pauli midfielder, who dispatched a dipping left-footed effort past Wang Dalei.
More joy came from the Australia right flank when Miller fired in a low cross in the 28th minute.
Velupillay was left unmarked on the penalty spot and when the ball deflected his way, the Victory winger powered a downward shot towards the Chinese goal.
Wang fumbled the ball into his own net to give Australia a 2-0 lead heading into half-time.
There was a brief Chinese fightback early into the second half but both efforts - a Li header and a shot from recently naturalised Brazilian-born playmaker Serginho - were easily dealt with by goalkeeper Maty Ryan.
It secured just the second cleansheet of the Popovic reign.
Irvine, who was named player of the match for a second game running after scoring twice in the 5-1 win over Indonesia, said: "We came with a top mentality into this camp and we knew what was at stake, two massive games for us."
