The direction was given on Wednesday by a bench headed by Chief Justice Mohit Shah, while hearing a petition filed by National Confederation for Development of the Disabled.
The quota would have to be applied in both recruitments and promotions.
The PIL seeks implementation of quota with effect from 1996 when the Act came into force. However, the bench has directed its implementation from 2010, when the PIL was filed.
Earlier, the state government had said that the issue fell within the domain of Union Public Service Commission and the Centre.
Counsel for the petitioner, advocate Mahesh Jethmalani, argued that section 33 of the Act clearly laid down that three per cent posts would be reserved for handicapped in every government establishment.
Jethmalani also referred to a Supreme Court judgement of 2010 which had said the rule would be applicable in direct recruitments and promotions.
The petitioner is this case was a handicapped person and an IAS candidate. The Government Counsel Rajiv Chavan agreed with the contention and said that in the wake of the apex court's judgement, the quota for the handicapped would be applicable to all the categories of posts.