Jean Uwinkindi organised and participated in attacks on the minority Tutsi ethnic group, the court ruled.
Some 800,000 Tutsis and moderate Hutus were killed by militias from the majority Hutu ethnic group.
The 64-year-old Hutu pastor was the first genocide suspect to be sent back to Rwanda for trial by the Tanzanian-based UN tribunal.
The tribunal shut down this month after sentencing 61 individuals and acquitting 14 others.
Uwinkindi - the former head of a Pentecostal church on the outskirts of the capital, Kigali - had opposed his transfer.
He said he would not get a fair trial in Rwanda, where there is now a Tutsi-led government.
His lawyers said he would appeal against the High Court's ruling.
"The court finds that there were killings of the Tutsi at Rwankeri and Kanzenze hills and that the attacks were led by Uwinkindi," said Judge Kanyegeri Timothee, Reuters news agency reports.
The prosecution alleged that in investigations after the genocide, some 2,000 bodies were found near the church in Kanzenze, just outside Kigali, where Uwinkindi was pastor.
He was indicted in 2011 after he was arrested in 2010 in neighbouring Uganda.
Another key suspect, Ladislas Ntaganzwa, who has a $5m (Â£3.2m) US bounty on him, was arrested two weeks ago in neighbouring Democratic Republic of Congo.

Officers forced entry to the house in Wood End Lane, Northolt, west London, at about 20:10 BST and detained a man in his 40s.
They say a search of the house is under way to make sure it is safe so that evacuated neighbours can return home.
Police said negotiations with the man had been unsuccessful.
A cordon of 200m had been in place at Wood End Lane since 01:00 BST on Friday, which was extended to 300m on Saturday.
About 80 residents have had to spend two nights away from their homes as officers negotiated with the man.
Scotland Yard said officers from the Territorial Support Group were supported by the London Fire Brigade as they moved in on the address.
Ch Supt Paul Martin said: "I am really pleased that this incident has now ended, and importantly ended without anyone coming to harm.
"Our key priority throughout this was to get the man out of the address safely as we had growing concerns about his well-being and believed him to be in crisis.
"After attempts to negotiate over a number of days did not work we used specialist officers to work out how we could gain entry to the address as safely as we could. They did that this evening."
Ch Supt Martin said police had also worked closely with the ambulance service and the local authority during the operation.
Searches of the property will be conducted "as quickly as we can to make sure people get home", he added.
Police had said there was no suggestion the incident was terror-related or linked to any ongoing police operations or investigation.

The new console will be released in the UK on 3 March and will cost UK gamers Â£279.99.
There are more than 80 games currently being developed for the console, but big names like Super Mario and The Legend of Zelda have been confirmed.
In October 2016, we got our first proper look at the console, and we compared it to some of the other top consoles available.
Rwanda's High Court has sentenced a pastor to life in prison for his role in the 1994 genocide.
[NEXT_CONCEPT]
A three-day stand-off between armed police and a man feared to have stockpiled petrol at his home has ended after officers entered the property.
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Nintendo has revealed lots of new details about its brand new console, the Nintendo Switch.