The Ospreys will make their St Helen's debut in late October against the Dragons in the United Rugby Championship.
Redevelopment work will begin at St Helen's this summer following joint investment from the Ospreys and Swansea Council. St Helen's will be the Ospreys' third home in as many seasons, having left the Swansea.com Stadium to play in the Bridgend's Brewery Field.
The Ospreys will start the season with a tour of South Africa where they will take on the Sharks and the Lions before a derby against the Dragons at Rodney Parade on October 9.
There will then be a European break before they play their first home URC fixture against the Dragons on Saturday, October 24 at 7.45pm. Win free tickets to watch Fiji v Wales in Cardiff this summer
The redevelopment of St Helen's had been delayed due to the Welsh Rugby Union initially refusing to provide guarantees surrounding the Ospreys' long term future, with plans still in place to cut the number of professional clubs in Wales from four to three.
Swansea Council took legal action against the WRU because they believed the governing body were using the potential Y11 purchase of Cardiff to turn the Ospreys into a semi-professional Super Rygbi Cymru outfit.
In the end Y11 decided not to go ahead with plans to buy Cardiff and the WRU announced it would retain four sides for the next two years.
This has meant the first phase of the redevelopment of St Helen's has now been given the go ahead.
Elsewhere, the Scarlets start with what should be a mouthwatering Welsh derby against Cardiff in Llanelli while the Dragons start with a trip to Benetton.
The traditional Boxing Day Welsh derbies are retained with the Dragons locking horns with Cardiff at Rodney Parade and the Ospreys hosting the Scarlets at St Helen's.
The format of the competition remains unchanged, with the top eight teams progressing to the play-Offs.
The Quarter-Finals will begin on Friday, May 28, with the Semi-Finals taking place from Saturday, June 5 before the Grand Final on Saturday, June 19 to crown the 2026/27 champions.
United Rugby Championship fixtures
Round one (all times in BST or GMT)
Friday, 25 September
Benetton v Dragons (19:45) Stadio Monigo, Treviso
September, 26 September
Sharks v Ospreys (15:00) Kings Park, Durban
Scarlets v Cardiff (19:45) Parc y Scarlets, Llanelli
Round two
Friday, 2 October
Cardiff v Zebre (19:45) Cardiff Arms Park, Cardiff
Saturday, 3 October
Lions v Ospreys (12:45) Ellis Park, Johannesburg
Dragons v Scarlets (15:00) Rodney Parade, Newport
Round three
Friday, 9 October
Dragons v Ospreys (19:45) Rodney Parade, Newport
Saturday, 10 October
Scarlets v Benetton (17:30) Parc y Scarlets, Llanelli
Leinster v Cardiff (19:45) Laya Arena, Dublin
Round four
Friday, 23 October
Cardiff v Sharks (19:45) Cardiff Arms Park, Cardiff
Saturday, 24 October
Stormers v Scarlets (15:00) DHL Stadium, Cape Town
Ospreys v Dragons (19:45) St Helen's, Swansea
Round five
Saturday, 31 October
Bulls v Scarlets (15:00) Loftus Versfeld, Pretoria
Dragons v Zebre (17:30) Rodney Parade, Newport
Ospreys v Cardiff (19:45) St Helen's, Swansea
Round six
Friday, 4 December
Ospreys v Leinster (19:45) St Helen's, Swansea
Edinburgh v Dragons (19:45) Hive Stadium, Edinburgh
Saturday, 5 December
Cardiff v Ulster (15:00) Cardiff Arms Park, Cardiff
Scarlets v Connacht (17:15) Parc y Scarlets, Llanelli
Round seven
Friday, 18 December
Ulster v Ospreys (19:45) Affidea Stadium, Belfast
Munster v Scarlets (19:45) Virgin Media Park, Cork
Saturday, 19 December
Cardiff v Dragons (15:00) Cardiff Arms Park, Cardiff
Round eight
Saturday, 26 December
Dragons v Cardiff (15:00) Rodney Parade, Newport
Ospreys v Scarlets (17:30) St Helen's, Swansea
Round nine
Saturday, 2 January
Scarlets v Dragons (15:00) Parc y Scarlets, Llanelli
Cardiff v Ospreys (17:30) Cardiff Arms Park, Cardiff
Round 10
Friday, Janurary 22
Glasgow Warriors v Scarlets (7.45pm) Scotstoun Stadium, Glasgow
Saturday, January 23
Ospreys v Edinburgh (3pm) St Helen's, Swansea
Leinster v Dragons (5.30pm) Laya Arena), Dublin
Round 11
Friday, January 29
Dragons v Munster (7.45pm) Rodney Parade, Newport
Glasgow Warriors v Ospreys (7.45pm) Scotstound Stadium, Glasgow
Saturday, January 30
Lions v Cardiff (12.45pm) Ellis Park, Johannesburg
Scarlets v Edinburgh (3pm) Parc y Scarlets, Llanelli
Round 12
Friday, February 26
Dragons v Ulster (7.45pm) Rodney Parade, Newport
Saturday, February 27
Cardiff v Glasgow Warriors (3pm) Cardiff Arms Park
Zebre Parma v Scarlets (5.30pm) Stadio Lanfranchi, Parma
Ospreys v Connacht (5.30pm) St Helen's, Swansea
Round 13
Friday, March 19
Connacht v Cardiff (7.45pm) Dexcom Stadium
Saturday, March 20
Vodacom Bulls v Dragons (3pm) Loftus Versfeld, Pretoria
Munster v Ospreys (5.30pm) Thomond Park, Limerick
Scarlets v Lions (5.30pm) Parc y Scarlets, Llanelli
Round 14
Friday, March 26Scarlets v Leinster (7.45pm) Parc y Scarlets
Saturday, March 27
Hollywoodbets Sharks v Dragons (4.30pm) Hollywoodbets Kings Park, Durban
Cardiff v Munster (5.30pm) Cardiff Arms Park
Ospreys v DHL Stormers (7.45pm) St Helen's, Swansea
Round 15
Friday, April 16
Dragons v Glasgow Warriors (7.45pm) Rodney Parade, Newport
Edinburgh v Cardiff (7.45pm) Hive Stadium, Edinburgh
Saturday, April 17
Ospreys v Vodacom Bulls (5.30pm) St Helen's, Swansea
Ulster v Scarlets (7.45pm) Affidea Stadium, Belfast
Round 16
Friday, April 23Zebre Parma v Ospreys (6pm) Stadio Lanfranchi, Parma
Cardiff v Vodacom Bulls (8.05pm) Cardiff Arms Park
Saturday, April 24
Scarlets v Hollywoodbets Sharks (3pm) Parc y Scarlets, Llanelli
Connacht v Dragons (7.45pm) Dexcom Stadium (Galway)
Round 17
Friday, May 7
Dragons v Lions (7.45pm) Rodney Parade, Newport
Saturday, May 8
Scarlets v Ospreys (5.30pm) Parc y Scarlets, LlanelliBenetton v Cardiff (7.45pm) Stadio Monigo, Treviso
Round 18
Friday, May 14Ospreys v Benetton (7.45pm) St Helen's, Swansea
Saturday, May 15Cardiff v Scarlets (3pm) Cardiff Arms Park
Dragons v DHL Stormers (5.30pm) Rodney Parade (Newport)