Following a pilot project in the Highlands, the initiative will be open to applicants nationwide from Autumn 2018 and will support people over the next three years.
In addition, a Challenge Fund to support pilot projects that will help to expand the custom and self-build sector is now open for applications until 01 December.
Minister Stewart said the early announcement on the national roll-out is being made after there was "considerable interest" in the fund following the pilot's launch in the Highlands.
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"We know many people seeking to build a bespoke home, which is tailored to their family needs, can find it tough getting the right advice and securing funding," he said.
"A pilot in the Highlands is proving to be really successful and now others in communities across Scotland will be able to apply for a share of this £4 million investment later next year.
"There was considerable interest in the fund following the launch of the pilot in the Highlands, which is why we have made the decision to make an early announcement on the national roll-out. This will give potential applicants the time to investigate housing plots and obtain the necessary permissions, so they can be ready to apply to the fund when it opens.
"In addition to this, our custom and self-build challenge fund is now open to support projects that will help planning departments develop ways to better respond to the needs of people undertaking a custom or self-build home."
(LM)
