With Edwin van der Sar sidelined he had the chance to stamp his authority on the Manchester United first team and with England lacking a dominant keeper, he could also have buttoned down a place in Fabio Capello's World Cup squad.
He's let the opportunities slip through his grasp and he's beginning to find out what it means to be a Manchester United player. Old Trafford's 'Theatre of Dreams' can become a nightmarish graveyard for men who aren't big enough to cope with its expectation levels.
It simply hasn't been a good start to the season for the 26-year-old who, at that age, should be reaching his peak.
United report that a chest injury prevented him training late last week. It might have been a factor in his poor performance against Sunderland but the image will still linger in the minds of most people of a 6ft 2in, 12st 8lb goalkeeper being outjumped and outmuscled by Kenwyne Jones for the visitors' second goal.
A confident keeper, having decided to come out for the ball, would have cleared out leather, bone and sinew - anything in his way - to get it away.
But Foster is clearly not buoyed by confidence. It wasn't his first mistake this season. There have been other high profile errors against Chelsea in the Community Shield and Manchester City in the derby. It isn't his first injury either. He missed England's August friendly with a knee problem.
It has to be a growing concern for Sir Alex Ferguson and Fabio Capello that he hasn't played enough football. Since signing professional for Stoke seven years ago, he's only managed 124 first team games. Knee, ankle and hand injuries have blighted him.
He was sent to Watford for two seasons to toughen up and gain more experience. He excelled there. United seemed to have made the right choice over a long-term replacement for Van der Sar. He has all the attributes to prove them right except one - Foster needs to grow into his United shirt.
The club's history is littered with fine players who simply couldn't cope with life under the Stretford End microscope.
Garry Birtles had a league scoring ratio of one every 2.7 games at Nottingham Forest before moving to United where he only netted every five games.
Foster has all the talent he needs and it would be a crying shame to see it go to waste
Peter Davenport scored 16 goals in his first season, but then faded. Kleberson won a World Cup with Brazil but couldn't cope with two years at United for whom he played just 30 games. The club took a reported £4m loss on him.
Eric Djemba Djemba was a £3.5m misfit and at £28.1m, Juan Sebastian Veron came with a massive global reputation but did not live up to it.
Goalkeepers? They've had a few, but then again too few to mention in glowing terms.
Fabien Barthez had a good title-winning year in 2001 before the cracks appeared against Deportivo La Coruna and Arsenal the following season.
For every great save like the one against Liverpool's Didi Hamann, a comic caper followed. Massimo Taibi's calamitous display in the 5-0 defeat at Chelsea was one of the worst I've seen from any keeper, anywhere.
To understand how they could have possibly failed at a club of such great tradition with such magnificent players around them, the exhausting burden of that tradition has to be taken into consideration along with the suffocating experience of having to play every game like a cup final under the glare of a worldwide audience.
It was interesting to read Michael Owen's comments last week explaining that at United you are expected to play at the top of your game in every match.
No other club in this modern age has enjoyed United's success. No other club's players are expected to repeat that success again and again and again. The pressure must be mind-rattling. The demands laid down by Sir Alex Ferguson must be daunting. But that's why he's a winner. Losers fall by the wayside.
However, others in the current squad have managed it.
Darren Fletcher had to withstand dog's abuse from his own fans in the early days, Rio Ferdinand had uncomfortable days after his move from Leeds, and Cristiano Ronaldo's first season was underwhelming. Strength of character and positive thinking got them through. These are the qualities Foster now needs, and quickly.
With Van der Sar expected back in the coming weeks, the Leamington Spa-born keeper will probably find himself understudy again. He has no chance of playing in the World Cup finals unless he's a first team regular. He and United will have big choices to make.
Reports suggest that Old Trafford keeper's coach Eric Steele has been "hard" on the player. He has to be.
Foster has all the talent he needs and it would be a crying shame to see it go to waste.
He can go on to become the long-term number one for club and country, but the club may not be Manchester United.
This page is best viewed in an up-to-date web browser with style sheets (CSS) enabled. While you will be able to view the content of this page in your current browser, you will not be able to get the full visual experience. Please consider upgrading your browser software or enabling style sheets (CSS) if you are able to do so.