The Bolton loanee grabbed his third goal for the club and second since re-signing on loan as Latics held on to a valuable three points.
The result saw Athletic move up to 13th position in the Sky Bet League One table.
Latics started the game sharply and could have taken the lead in the opening five minutes.
Rhys Turner broke the offside trap, raced at the last defender and saw his shot tipped wide from former goalkeeper Paul Rachubka.
Latics were being cheered on by the 737 fans, who were in fine voice throughout the half.
Crewe grew into the game and had their best opportunity on 10 minutes through the dangerous Nicky Ajose.
The man, who bagged two in the earlier fixture between the two, broke through Latics' rearguard but chipped his shot over the crossbar.
Latics raced up the other end and forced a corner which was flicked on at the front post by new loan signing Anthony Gerrard but Jonathan Forte could not tap home from inside the six yard box.
Turner was proving a handful in attack in only his second start of the season and he nipped in front of his defender but just headed over the crossbar on 15 minutes.
The pressure was coming from the visitors and Forte could have put Latics ahead but the linesman's flag prevented the chance.
Coleman, who was making his first professional start, grew as the half went on and was out quickly to deny Ajose a chance to shoot.
With under ten minutes of the first half remaining, Connor Brown picked up his fifth booking of the season after halting Anthony Grants run down the left-hand side.
Both sides had chances before the break to take the lead. Firstly Danny Philliskirk latched onto Mike Jones' through ball but Rachubka denied him.
Seconds later, at the other end, Marcus Haber went down under a challenge from Adam Lockwood but the referee waved the penalty protests away.
Latics came out firing in the second half but Mike Jones' ambitious strike on 47 minutes did not trouble Rachubka.
Athletic were enjoying a lot of the possession in the early parts of the second half but they could not make their crosses into the box pay.
Coleman was forced into action just before the hour mark as he tipped over a shot from Crewe midfielder Grant.
The goalkeeper excellently denied him from 25 yards but worrying signs followed as he stayed down but after lengthy treatment he was alright to continue.
Conor Wilkinson entered the action in place of Rhys Tuner on 64 minutes and partnered Forte in attack for the final 25 minutes.
Coleman had to be alert on 70 minutes as James Jones' strike for Crewe took a wicked deflection which wrong-footed him but he saved well on the line.
Two minutes later, Latics took the lead through Wilkinson.
Neat work on the left-hand side presented Philliskirk with a sight of goal but his shot was parried by Rachubka.
Forte kept the ball alive and played the ball back to Philliskirk who guided the ball into the path of Wilkinson who finished from inside the box to send the travelling supporters into delirium.
The ascendancy was with Latics and they could have extended their lead ten minutes from time but Woodland's shot goalwards was just blocked at the last.
Crewe threw everything forward in a bid to get something out of the game but Latics' defence stood resolutely with Gerrard a colossus at the heart of the back four.
After a late flurry of corners, Latics held on to the vital three points to seal Holden's second victory as boss.
Crewe Alexandra: Rachubka, Guthrie, Davis, Turton, Jones, Leigh (Cooper 88'), Haber (Ikpeazu 69'), Ness, Tate (Dalla Valle 80'), Ajose, Grant.
Subs not used: Nolan, Baillie, Stewart, Atkinson.
Oldham Athletic: Coleman, Brown, Gerrard, Lockwood, Sadler, Woodland, Winchester, Jones, Forte, Philliskirk, Turner (Wilkinson 64').
Subs not used: Tyson, Dieng, Kusunga, B.Wilson, Mellor, Jacobs.
Goals: Crewe Alexandra 0-1 Oldham Athletic (Wilkinson 74')
Attendance: 4,669 (737 visiting supporters)