Chris Taylor struck an 84th-minute winner as Oldham overturned a 3-1 deficit to settle an incredible game that produced seven goals, six bookings and a controversial red card for Lions skipper Paul Robinson.
Millwall looked to be in complete control as Kenny Jackett's side established a 3-1 lead after 56 minutes and there appeared to be no way back for Oldham.
But a triple substitution on the hour by Latics' boss John Sheridan followed by Robinson's dismissal for a foul on Lee Hughes saw the tide turn Oldham's way.
Andy Liddell reduced the deficit from the resulting spot-kick and 10-man Millwall were undone by two further goals in the last 11 minutes firstly from sub Lewis Allesandra before Taylor fired home the clincher.
It had started so well for the visitors when Tresor Kandol marked his Lions debut with a goal after just 13 seconds, glancing a header home from Alan Dunne's right-wing cross.
The celebrations amongst the travelling fans were cut short two minutes later when Liddell met Kevin Maher's free-kick to head home the equaliser.
Back came The Lions and when Mark Crossley and defender Rueben Hazell got in each other's way in the 13th-minute the ball bounced off Hazell's shoulder and floated into the back of the net.
Lewis Grabban looked to have put Millwall on the way to their first opening day win in five years when he steered home a third goal 56 minutes after Dave Martin's shot was touched onto the post by Crossley.
But then the game was turned on its head when Robbo was harshley penalised for a foul on sub Hughes and shown a straight red card by referee Nigel Miller, whose last game officiating The Lions came at Coventry City in the FA Cup last season.
Liddell smacked home the resulting penalty and it was game on as Millwall found it difficult to cope with a rejuvenated Oldham side.
Fellow sub Allesandra fired the hosts level 11 minutes from time with a goal that had a suspicion of offside about it before Taylor sent the home crowd wild with a neat finish following a well worked free-kick to compound Millwall's misery.

Oldham Athletic: Crossley, Eardley, Hazell, Gregan, Lomax, Liddell, Allott, Maher (Whitaker, 61mins), Taylor, O'Grady (Hughes, 61mins), Davies (Allesandra, 61mins). Subs not used: Fleming, Stam.
Bookings: O'Grady (38mins), Liddell (42mins), Taylor (84mins)
Scorers: Liddell (2mins, 73mins pen), Allesandra, 79mins), Taylor (84mins)

Millwall: Forde, Dunne (Hackett, 80mins), Craig, Laird, Robinson, Whitbread, Fuseini, Grabban, Kandol (Alexander, 83mins), Martin, Abdou (Frampton, 75mins). Subs not used: Edwards, Brkovic.
Bookings: Abdou (7mins), Dunne (43mins), Whitbread (83mins)
Sent off: Robinson (73mins)
Scorers: Kandol (13secs), Hazell (og 13mins), Grabban (56mins)

Ref: N Miller
Att: 5,367 (away 510)