The girls, aged 13 to 16, from Agryz, a small town of 19,000 people some 800 km (500 miles) east of Moscow, were selected by the Russian national team after making a sponsor's shortlist of "inspiring entrants" to a national junior football tournament.
"It's like a fairytale for them", said their coach, Ildar Idiyatov.
The 14 girls, who play football for a team in the Russian region of Tartarstan, will have the eyes of the world on them as they return the ball in the Group A match between Russia and Saudi Arabia at the Luzhniki Stadium in Moscow.
The local World Cup organising committee said 776 children would work as ballboys and ballgirls at the 64 match tournament, but this was the first time an all-female group had operated at the opening game of the FIFA showpiece.
"Women are not a weak sex, we are always ready to compete with boys at the same level," said Daria Vasilyeva, one of the ball girls selected for the opening match.
"At the World Cup, all of us are united and we are all just as worthy and can also pass the balls to the football teams."
(Writing by Patrick Johnston in LONDON; Editing by Alison Williams)
