The forward struck from 30 yards, and with a good bit of fortune, the ball found a way into the back of the net for Latics to seal the three points.
Chesterfield had taken the lead in the first half through a Sylvain Ebanks-Blake strike but Latics levelled the game through Dominic Poleon with less than 20 minutes to go.
Latics’ winner came three minutes from time and takes them up to 18th in the Sky Bet League One table.
David Dunn made two changes to his starting 11 as Liam Kelly and James Wilson returned for Cameron Dummigan and Ricardo Fuller.
Latics started the game brightly but it was Chesterfield that had the first opportunity of the game through Ebanks-Blake.
The striker let fly from 25 yards but it did not trouble Latics goalkeeper Joel Coleman.
Athletic broke instantly and Winchester struck wide from 30 yards but went wide of Tommy Lee’s goal.
The visitors were knocking the ball around well in midfield but were struggling to find the finishing touch in front of goal.
A free kick from 18 yards was taken by Mark Yeates on 17 minutes but Lee saved well at his far post to deny the winger.
On the half hour mark, Chesterfield should have taken the lead through central defender Ian Evatt.
The defender was allowed space inside the penalty area but his mis-kicked his shot and the chance was lost.
However, one minute later, the Spireites did get their noses in front through Ebanks-Blake.
The striker met a cross into the box and guided into the goal from six yards as Latics fell behind.
Latics almost hit back instantly but Liam Kelly’s strike from 25 yards deflected inches over the crossbar.
With Latics attacking, they were almost caught on the break five minutes before half time but Brian Wilson got back to deny Dan Gardner from 10 yards.
Liam Kelly won a free kick 30 yards from goal minutes before the half time whistle but Joseph Mills’ strike went well wide of the goal.
Dunn must have had a strong word with his players at the break as they came out attacking in the second half.
As the conditions started to play a part in the game, Poleon almost capitalised as a through ball bypassed the central defenders but Lee was out to head clear.
Latics had the better of the ball in the opening exchanges of the second half and on the hour mark, Yeates fired at goal but Ian Evatt managed to get a block in.
Minutes later, Winchester stung the palms of Lee as Latics continued to press forward in a bid to get an equaliser.
Dunn made a double change and introduced Jay Fulton and Giorgio Rasulo into action.
That change paid dividends for Athletic as Rasulo’s shot from 25 yards was spilled by Lee into the path of Poleon who knocked over the line to equalise for Latics.
Athletic were full of confidence after the goal and they went in search of a winner with 18 minutes of the game remaining.
The changes made a positive impact and Rasulo was proving positive on the ball and at the centre of all the action.
Poleon turned his man on 80 minutes but had his shot blocked as Latics went in search of more goals.
He again found himself behind the defence with five minutes remaining but he dragged his shot past Lee’s far post.
They had to be wary at the other end, however, as Dan Jones struck the crossbar from a long cross into the box.
With only three minutes of the game remaining, Latics did find the winner, which was deserved based on their second half performance.
Philliskirk blasted from 30 yards, and after a fumble from Lee, it found a way into the back of the goal and sent the Latics supporters into a state of ecstasy.
It could have three only two minutes later as Rasulo’s inch-perfect through ball found Poleon to chase but his shot was blocked at the last.
Latics defended manfully in the final four minutes of the game and came out with the valuable three points.
Chesterfield: Lee, Talbot, Evatt, Wood (Raglan 90’), Jones, Morsy, Herd (Ariyibi 90’), O’Shea, Gardner (Simons 80’), Novak, Ebanks-Blake.
Subs not used: Hird, O’Neil, Banks, Dieseruvwe.
Oldham Athletic: Coleman, B.Wilson, Dieng, J.Wilson, Mills, Kelly, Winchester (Rasulo 69’) L, Yeates, Poleon, Philliskirk, Higdon (Fulton 69’).
Subs not used: Renshaw, Eckersley, Brown, Vassell, Fuller.
Goals: Chesterfield (Ebanks-Blake 34’) 1-2 Oldham Athletic (Poleon 72’, Tommy Lee OG 87’)
Attendance: 6,178 (445 visiting supporters)