Former wheelclamper and bouncer Levi Bellfield abducted and murdered Milly, 13, then went on to murder two other young women and attempt to murder a third, a court heard.
Milly, who only took a different route home from school by chance that day, was "gone in the blink of an eye" in what was "every parent's worst nightmare", an Old Bailey jury was told.
Her decomposing body was not found until six months later in a field 25 miles away.
Brian Altman, QC, prosecuting, told the jury that the day before Milly went missing, Bellfield allegedly tried to abduct another schoolgirl in uniform a few miles away.
Bellfield, 42, formerly of West Drayton, west London, denies Milly's kidnap and murder after she left Walton-on-Thames train station in Surrey on March 21, 2002.
He also denies the attempted kidnap of 11-year-old Rachel Cowles, who was approached by a man in a red car in Shepperton, Surrey, on March 20, 2002.
Mr Altman said Milly, whose birth name was Amanda, had spent an ordinary day at school in Weybridge, Surrey.
Still in her uniform, she took a train with friends and spent time with them in the station cafe at Walton-on-Thames, where they ate chips.
Then she began to walk to her home about a mile away along Station Avenue, where Bellfield had been staying at the time in Collingwood Place, the court heard.
"Within moments of leaving the station to walk along the road, just a few minutes after 4pm, she vanished - gone in the blink of an eye," said Mr Altman.
"Milly had simply disappeared in a flash from a street in a suburban town in broad daylight.
"This was of course every parent's worst nightmare."
Mr Altman said it was only by chance that Milly was taking that route home.
She would normally have got off at another station but had gone to the cafe with friends that day.
Bellfield, wearing a dark-grey suit, sat in the dock as he listened to the opening of the case along with the five women and seven men of the jury.
The jury heard that Milly's disappearance sparked a major police hunt and months of agonising uncertainty for her family.
Mr Altman said: "For six long months the Dowler family suffered the excruciating pain of not knowing what had become of their daughter.
"On Wednesday 18th September 2002, some mushroom pickers found, quite by chance, the unclothed and badly decomposed body of a young female lying in the undergrowth of Yateley Wood in Hampshire."
The remains were identified as Milly but the cause of death could not be determined because of the length of time that had passed.
At the time Milly vanished, Bellfield was living with his partner, Emma Mills, and their two children in a rented ground- floor flat "just yards away from the spot where Milly was last seen alive".
Within 22 minutes of Milly disappearing, a red Daewoo Nexia car, which Bellfield was using at the time, was caught on CCTV leaving the area by the access road to the flats and along Station Avenue.
The day before, at around the some time, there had been an attempt to abduct another schoolgirl in Upper Halliford Road, Shepperton, 3.3 miles away.
Rachel Cowles was approached by a man in a small red car driven by a man resembling Bellfield, it was alleged.
Mr Altman said: "He tried tricking her by telling her that he had just moved in next door and asked her if she wanted a lift.
"Sensibly she did not accept his offer. At this time, a police car was driven along the road, which possibly spooked the man and he drove off.
"The prosecution say there can be no doubt that Levi Bellfield was responsible for both.
"He has been proven to be a predatory and violent offender towards women."
Bellfield had gone on to attack other women in west London over a period of just over two years and was convicted at the Old Bailey in 2008.
He killed Marsha McDonnell, 19, in February 2003 and Amelie Delagrange, 22, in August 2004, by striking them on the head with a blunt instrument.
In May 2004, he attempted to murder Kate Sheedy, 18, by deliberately running her over in a car.
Mr Altman said the offences bore "similarity in many respects" to Milly's murder and Rachel's attempted abduction.
Milly lived with her parents, Robert and Sally, and older sister, Gemma.
Mr Altman continued: "Milly was slim, pretty and intelligent. She was popular among her friends. To all intents and purposes she was an ordinary girl who was developing into a find young woman."
Jurors were told they would be visiting Walton-on-Thames and Shepperton on Thursday.
The court heard that on the day she disappeared, Milly had been due to get a lift home from school with her mother Sally, a teacher, and sister Gemma.
Mrs Dowler had a tutorial lesson at the end of the day while Gemma had PE practice and Milly had some artwork to finish after school.
But the schoolgirl told her mother she had done it during the lunch break so she was going to take the train home instead of waiting for her.
"To her mother, Milly seemed absolutely fine, and she was acting no differently to any other school day," said Mr Altman.
Jurors were shown footage from CCTV cameras of the teenager leaving school, going through ticket barriers at Weybridge station, and down a staircase onto the station platform.
The trial was adjourned until tomorrow.
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