For Miller, this was a breakthrough race - as it not only marked his first ever MotoGP win, but was also the first podium finish of his career and second top-ten finish in two years of top-class racing.
This marked the first time in ten years that a non-factory bike has won a MotoGP class race, and Miller was also the first Australian race winner since since Casey Stoner's victory at Phillip Island in 2012.
The weather played a major factor in Assen, as it caused problems for the riders throughout the race - with nine riders failing to finish the race due to the conditions.
In the early stages of the race, Yonny Hernandez appeared to be in control - as the Colombian rider held a comfortable two-second advantage ahead of the rest of the pack.
Just as the track appeared to be drying up - the heavens opened and the rain intensified, which caused problems for Hernandez, who slipped off his bike from the lead and fell into 16th position.
This allowed Ducati's Andrea Dovizioso to move into the race lead, with the Italian duo of Valentino Rossi and Danilo Petrucci in close pursuit.
Petrucci, known as a wet-weather specialist, made a bold move past Rossi and Dovizioso on Lap 14 to jump briefly into the race lead - but this was reversed when the race marshals threw up a red flag to stop the race until conditions cleared.
After a brief delay - the riders emerged from their garages and were ready for a race restart, which saw Dovizioso start the shortened 12-lap race on pole.
Miller began the restarted race in eighth position, but after a series of crashes from the Hondas of Dani Pedrosa and Cal Crutchlow - Miller quickly jumped into fourth, thriving as other riders struggled to adapt to the track conditions.
At the end of the opening lap, Rossi took the race lead , followed by Dovizioso, Marquez and Miller - as Bradley Smith crashed out of the race and Petrucci was forced to retire.
The chaos ensued, with Dovizioso succumbing to the wet weather, as he slid off his bike from second position - shortly followed by Valentino Rossi, who crashed despite leading the race.
The race was now between Marquez and Miller, who jostled for position for a few laps, before Miller made his decisive move with nine laps remaining to take the lead.
Miller made his move past Marquez with nine laps remaining (Photo by Bas Czerwinski/AFP/Getty Images)
As the laps ticked by, Miller's lead continued to grow - as Marquez seemed content to take second place and secure himself a 24-point cushion ahead of Jorge Lorenzo in the Championship race.
This allowed the 21-year-old Australian to ride into the distance and secure his breakthrough victory.
British rider Scott Redding completed the podium after a terrific ride on his Ducati, while Yamaha's Pol Espargaro finished fourth.
After starting the race from the back of the back, Ducati's Andrea Iannone finished fifth, while fellow Ducati's Hector Barbera and Eugene Laverty followed in sixth and seventh respectively.
Aprilia's Stefan Bradl finished eighth, while young Spaniard Maverick Vinales crossed the line in ninth on his Suzuki.
Yamaha's Jorge Lorenzo rounded out the top ten,