With Slovakia beating Malta 3-0, it left the Scots needing a win to seal runners-up spot and a playoff place from Group F. When Leigh Griffiths put Scotland ahead against the run of play in the first half, they were on course to do just that.
Yet after Slovenia's Roman Bezjak, who came on at the break, cashed in on poor defending from set pieces to head a 52nd minute equaliser and sidefoot a second after 72 minutes, Gordon Strachan's Scotland side needed a late surge to save the day.
Although substitute Robert Snodgrass snatched an 88th minute equaliser, Scotland never really looked good enough even when coming close to unlikely glory after Slovenia's Bostjan Cesar, on his 100th appearance, was sent off in added time.
After Cesar's red card following an altercation with Christophe Berra, Snodgrass could not generate enough power to direct his header over goalkeeper Jan Oblak, who had conceded his first goals at home in the qualifying campaign.
The draw meant Scotland finished third in the group on 18 points, behind Slovakia on goal difference, eight points adrift of group winners England and three points ahead of Slovenia.
The result also confirmed Northern Ireland's place in the playoffs, as the Group C side have a better record against the teams in their section than Slovakia have in Group F.
Europe's nine group winners qualify automatically for next year's 32-team tournament in Russia, while the eight best runners-up enter a two-leg playoff for the last four berths.
Unsurprisingly, Griffiths had looked as if he could again be Scotland's hero when his 32nd minute left-foot strike from an unpromising narrow angle beat the excellent Oblak.
It was the Celtic striker's fourth goal in his last five Scotland games and had the 'Tartan Army' of travelling fans believing in the dream of reaching the finals, being held in Russia next year, for the first time in two decades.
"But two lapses of concentration have cost us," said Griffiths. "For all the possession they had, they didn't really cut us open. Two set pieces have cost us dearly."
Strachan, whose future as manager remains uncertain, paid tribute to his side, saying: "It's an honour to be their coach. This group of players is as good as any I've worked with."
(Reporting by Ian Chadband; Editing by Christian Radnedge and Ken Ferris)
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