In a country where women face a host of restrictions including a driving ban, the move was welcomed as an important step forward.
But it also faced criticism from hardline conservatives and from rights groups who said it does not go far enough in providing women with equal rights.
It came after another first earlier this month, when women started to register as voters for the December local elections at centres run by all-female staff, separate from registration facilities for Saudi males.
Women in the oil-rich Gulf state, which applies a strict segregation of the sexes, are banned from driving and have to cover themselves in public from head to toe.
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They also have to obtain the consent of a male guardian to travel, work, apply for a passport or to marry.
The late king Abdullah in 2011 granted women the right to vote and to stand as candidates in this year's local elections.
Candidate registration is to run until September 17, while voter registration ends on September 14.
Out of 1,263 polling stations in 284 municipalities across the monarchy, 424 have been reserved for women voters.
"I am very excited to take part in this new experience," said Amal Mohammed, 35, as she registered to vote in the port city of Jeddah.
Abdullah, who died in January and was succeeded by King Salman, introduced municipal elections to Saudi Arabia in 2005 when he was crown prince.