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The result leaves Celtic with no points from six after two league-phase fixtures in the Europa League and means they have now lost four of their last five matches across all competitions.
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Another defeat - fairly or unfairly - also raises more questions over O'Neill's future in the Parkhead hot seat.
It was just weeks ago, following consecutive defeats to Rangers and a loss in their opening Europa League fixture, that O'Neill said he was going to consider his position after a gruelling week. He stayed, and now he must deliver.
Here we answer some key questions as the veteran boss chases another huge result on Sunday...
Sunday 18th October 2:30pm
Kick off 3:00pm
What did O'Neill say in Lisbon?
Following that 4-1 thumping against Benfica, O'Neill hailed Celtic's second-half display and believes they can still progress in the competition despite sitting 34th in a 36-team table.
"The last thing you want to do is concede so early on," he told TNT Sports. "Then at 2-0 we've got a great, great chance to make it 2-1 and within a few minutes they make it 3-0.
"We could have capitulated, but I thought the second-half performance was really terrific. It was a game of two halves. We created chance after chance, we should have scored more goals.
"The second-half performance gives me what I would call the determination, and I think we can still qualify. I know it's down to six games, but we want to qualify for this competition to get into the knockout stages.
"Overall, I'm really, really delighted with the second-half performance, and it's a shame that we conceded the three goals first of all."
Does O'Neill have a point?
Benfica were clinical and ultimately too much to handle.
In the first half, even when Celtic were not causing their own problems, such as giving away a penalty for the hosts' opener, they were being cut apart at times. That's where the problem lies.
Yes, O'Neill's side could have scored when they hit the frame of the goal in either half - but so could have their opponents.
Yes, things did improve after the restart - but could it have got any worse considering the Hoops were 3-0 down after 36 minutes?
O'Neill may be using all of his managerial experience to try to motivate his side and create some positivity among the fans ahead of a huge game against Hearts. After all, he needs a raucous Parkhead on Sunday to help them get past last season's runners-up.
So those with a glass half-full mindset will be fully in favour of that. However, those with a glass half-empty approach will have been worried by Thursday and demand improvement. Quickly.
Losing in their Champions League qualifier, to Rangers in the Premiership and League Cup, and now another Europa League loss - the worrying trend of failure in big matches is something that needs to end.
Celtic's last five results
- Rangers 3-0 Celtic - League Cup
- Celtic 1-3 Ferencvaros - Europa League
- Celtic 0-1 Rangers - Scottish Premiership
- Motherwell 0-2 Celtic - Scottish Premiership
- Benfica 4-1 Celtic - Europa League
What is the fan view?
Speaking on Sky Sports News, Tino Callaghan from A Celtic Exchange Podcast said:
"They were the kind of comments I suppose you'd expect any manager to make. There are small positives to take from Celtic's second half, and I think the manager is choosing to accentuate them, which you would expect him to do.
"However, there was so much wrong in the first half in particular, and that's where the real issues are for Celtic at this moment in time.
"It's just the fact that at times we weren't even competing. We were completely outstripped in that first half, and I think that in itself points back to a more general feeling of frustration amongst the fans that we are no longer competing at the top table in Europe.
"Back in the day, we would potentially draw Benfica in the Champions League and fancy our chances of maybe getting something, but we went into that game last night with no real hope.
"I really thought he was going to leave after his comments after the Rangers game. They were particularly concerning. It's not that everyone else was asking the question. The man himself was asking the question of himself, and I thought there was a serious chance he would walk.
"It seems that he's taken some time to reflect. He's probably spoken to people at the club and decided to stay on, but you need to start getting results if you've decided that you are the man for the job.
"Hearts is massive now on Sunday. A must-win game. Martin O'Neill came out quite strongly, saying that he thinks we still can qualify in the Europa League too. I agree with that, but talk is cheap. You need to start doing it on the park, and that starts again on Sunday."
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Sutton: What does O'Neill have going for him?
Speaking before Celtic beat Motherwell, former Parkhead player and Sky Sports pundit Chris Sutton said:
"I thought he was wrong to say what he said in terms of he had doubts [about his future in the job]. People will view that as a weakness. I think that was a big mistake.
"I've never heard him talk like that in his whole managerial career. I just think, if I was Martin, I would just want an easy life. What has he got going for him at Celtic at this moment?
"He didn't get the players he wanted in order to compete at the highest of levels in Europe, so he was let down there. He was undermined by one of his players, Cameron Carter-Vickers, who shouldn't be coming out publicly and undermining the manager and questioning the tactics.
"It just shows where the club is at. It's like the Wild West, there are shots fired everywhere. You now have the situation where the Green Brigade are saying 'we are not going to rock up at European games. We aren't going to go to the cup games.'
"The split between the top of the club and the supporters, I thought couldn't get any wider than last year. It does seem now that it is more fractious." %!s(