The Australian, who learned his trade with the south Londoners, scrambled home the second half winner which finally subdued the Coca-Cola Championship side.
Everton certainly knew they had been in a game and struggled desperately in the first period.
The home side lost captain David Weir with blood pouring from a head wound and it was not until Cahill's strike that the Toffees got a grip on the game.
Everton started well with Leon Osman seeing a header fly over from Mikel Arteta's free-kick, before driving a 20-yard effort over the bar.
But Millwall's effort and pace constantly had Everton worried at the back, and the Lions responded with a hooked effort from Dunne which cleared the bar, before Ben May blasted a free-kick into the wall after Morris had been fouled by Ferrari.
Millwall goalkeeper Andy Marshall then made a brave save at the feet of James Beattie, but much of the action was still at the other end.
Everton came forward more after the break, but Millwall defended with resolve, with on-loan Liverpool centre-back Zak Whitbread at the heart of the defiance.
But the visitors needed Marshall to produce an instinctive, tip-over from Cahill's fierce header following an Osman cross from the right.
Kilbane then came close with a cross-shot from Osman's pass and went closer still with a header against a post following a corner.
But the breakthrough came 18 minutes from time when Arteta played in Beattie down the right. The striker squared the ball for Cahill to beat Marshall from just inside the box.
Three minutes later it could have been two when Beattie again provided the supply line and Neville saw a fierce header crash against a post. In the 77th minute Livermore forced Nigel Martyn into a sprawling save to his left, before Everton sub Kroldrup sent a powerful header just over the angle as the Toffees attempted to finish the game as a contest.
: Martyn, Hibbert, Weir (Kroldrup 33), Ferrari, Nuno Valente, Osman, Arteta, Neville, Cahill, Kilbane (McFadden 86), Beattie.
: Marshall, Robinson, Lawrence, Whitbread, Morris (Cogan 77), Dunne, Elliott, Livermore, Craig (Braniff 89), May, Williams.
: R Styles (Hampshire).
: AC Milan 1 Ascoli 0, Cagliari 1 Siena 0, Chievo 1 Juventus 1, Empoli 1 Udinese 1, Lecce 0 Livorno 0, Messina 1 Lazio 1, Palermo 4 Parma 2, Roma 3 Reggina 1, Sampdoria 3 Fiorentina 1, Treviso 0 Inter Milan 1.
: Real Betis 0 Real Madrid 1; Cadiz 0 Espanyol 2.
: Saudi Arabia 1 Sweden 1.
: Boston Utd 0 Carlisle 5.