The Burton full-back beat Steven Drench from the spot after Ged Brannan had handled the ball in the 77th minute. And that was enough for Burton's first-ever win over Morecambe in the Nationwide Conference - at the ninth time of asking.
Burton are a side that many people are tipping to do well this season in the Conference, buoyed by last season's FA Cup exploits which earned them a replay at Old Trafford against Manchester United.
That has helped manager Nigel Clough add to his squad, with his most high-profile capture being former Conference Golden Boot winner Daryl Clare, starting his first full season with the Brewers.
And Clare showed over these first 90 minutes of the season that he will be a threat to many a Conference defence again this campaign with a lively performance.
At the other end, the Brewers had to call on 43-year-old goalkeeper Kevin Poole to fill a hole left due to injuries.
Poole did well when he was needed, but to be fair he chose a quiet game to make his debut with the game having 0-0 written all over until Brannan's handball.
That capped a bad day at the office for Morecambe and manager Sammy McIlroy who gave a debut to new signing Craig Stanley in midfield.
Stanley started well playing the ball around in midfield as the home side looked to make early inroads against a side that they have always fared well against.
It was the former Hereford man who set up Michael Howard in the sixth minute, but the left-back's effort from range was straight at Poole.
Three minutes later, Burton's right-back Gary Rowett had a dip from distance too and his 35-yard shot forced Drench to tip the ball over the bar.
Webster shot straight at Drench with a free-kick and Darren Tinson's header went the same way as the visitors came into the game.
Howard raced back to deny Clare on 19 minutes before the striker did hit the back of the net with a great shot, but it was ruled out for offside.
Morecambe did not create many openings, their best of the opening periods coming in the 31st minute when a corner was headed back by Garry Thompson and Stanley's header was cleared off the line by Ryan Austin.
Andy Ducros shot wide for Burton and, at the other end, Jim Bentley headed off target before the referee blew for half-time.
Like the first half, Morecambe came out of the blocks the better in the second half and Michael Twiss got away but with little support, Poole was able to save his cross-shot.
On 56 minutes, Brannan's cross caused confusion in the Burton defence, the ball being scrambled away for a corner as Dave Perkins waited for a chance.
The key moment for Morecambe attacking wise came in the 58th minute.
Carlton controlled the ball, took aim and was ready to fire the Shrimps in front before Tinson slid in to deny him that shooting opportunity.
Thompson had a go with a 25-yard free-kick but his shot caught the wall and Poole was able to scramble across and push the ball clear.
That save proved important as two minutes later, in the 77th minute, Burton went up the other end and scored.
Ducros was a constant threat on the left and was looking ever more dangerous.
He got into the box and was nearly through but Brannan handled.
Referee Varley gave the penalty and Webster put it away to set up a historic win for the Brewers.
Morecambe tried to get back into the game but their only real effort on goal in the last 10 minutes was substitute David McNiven's header which went straight at Poole.