For much of a tense affair it looked as though Shamrock Rovers were going to deny put their celebrations on hold, with the home side looking comfortable from the moment Danny North put them in front just after half-time.
However, Pat Fenlon’s side pressed the self-destruct button in the 84th minute when Patrick Cregg dived in on Darren Meenan at the edge of the box as he was going away from goal with referee Padraig Sutton immediately pointing to the spot.
Towell then comfortably dispatched his effort to the bottom right hand corner to send the 800 travelling supporters into delirium.
It was the midfielder’s sixth penalty of a campaign which has seen him score 25 goals to date in all competitions and 22 in the league.
His goal, coupled with Cork City’s failure to win away to Drogheda Utd, meant an 11th league title for Stephen Kenny’s side.
Before Towell’s spot-kick it looked like Dundalk would have to wait at least another week to celebrate as the visitors never really looked like breaking through.
Despite being the league’s outstanding performers this season, the Lilywhites struggled to get going in the game with Rovers creating the better chances right from the off.
Andy Boyle was called into action to block a Gavin Brennan shot inside the opening two minutes while Mikey Drennan volleyed just over from a Dave O’Connor cross on 19 minutes.
In between Ronan Finn looked to have been slipped in on goal by Meenan but his effort was well blocked down by Maxime Blanchard.
Just after the half hour mark Drennan went close again with a downward header from Brandon Miele’s fizzed cross but the former Aston Villa man would have a major say in the opener just 19 seconds after the restart.
His exquisite pass released Miele on the left. The winger’s shot was blocked by the legs of Rogers but the loose ball fell inviting to North who smashed home from close range.
Dundalk pressed hard for an equaliser after that but despite two efforts from captain Stephen O’Donnell they never really looked like getting the breakthrough.
Their best chance fell Finn’s way on 77 minutes when he was picked out by Dane Massey’s cross but his speculative flick was well over.
Dundalk were thrown a lifeline seven minutes later though when Cregg’s foul presented them with a spot kick that Towell never looked like passing up.
And, after a tense wait on the full-time whistle from United Park, the celebrations commenced.
Now the Lilywhites go in search of a double when they meet Cork City in the FAI Cup on November 8th.
Regardless of the result in that game, the squad of 2015 have ensured their place amongst the greats to have donned the white jersey.
Murphy; Madden, Blanchard, Webster, O’Connor; Cregg, McCabe; G Brennan, Drennan, Miele; North (R Brennan 79). Subs not used: Hyland, Kenna, McPhail, Waters, Duff, McCaffrey.
Rogers; Shields, Barrett, Boyle, Massey; Meenan, O’Donnell, Towell, Horgan (Mountney 61); Finn (Byrne 83); McMillan (Kilduff 65). Subs not used: Sava, Grimes, Finnegan, O’Connor.
P Sutton (Clare).