St. John's County Homes With Guest Suite

Are you a home buyer who could use the extra living space a guest suite provides? Featured here are all St. John's County homes for sale with a guest suite. If you’re interested in any of the St. John's County guest suite home listings that you see below, just click the "Ask a Question" button when viewing the details of that property. Our St. John's County real estate agents can provide you with disclosures, past sales history, dates and prices of properties recently sold nearby, and other details related to St. John's County homes with a guest suite.

And if you'd like to stay up-to-date on St. John's County homes with a guest suite, we also invite you to register for a free account so that you can receive email alerts whenever new listings hit the market that fit your search criteria, allowing you to stay one-step ahead of other buyers in the area. And remember to call or text us directly with any additional questions you have about buying or selling a home in St. John's County, Florida. 

Search St. John's County Homes With Guest Suite

Click the links below to sort results by price range.

Sort by:
New
68 Reunion Trl, PONTE VEDRA

$650,000

68 Reunion Trl, PONTE VEDRA

4 Beds 3 Baths 2,085 SqFt Residential MLS® # 1229384
New
121 Twilight Tear Way, ST JOHNS

$764,827

121 Twilight Tear Way, ST JOHNS

5 Beds 5 Baths 3,529 SqFt Residential MLS® # 1229347
New
1351 Ivyhedge Ave, ST AUGUSTINE

$508,000

1351 Ivyhedge Ave, ST AUGUSTINE

4 Beds 3 Baths 2,401 SqFt Residential MLS® # 1229277
New
261 Dosel Ln, ST AUGUSTINE

$740,000

261 Dosel Ln, ST AUGUSTINE

4 Beds 3 Baths 2,689 SqFt Residential MLS® # 1229232
New
36 Lochnagar Mountain Dr, ST JOHNS

$550,000

36 Lochnagar Mountain Dr, ST JOHNS

4 Beds 4 Baths 2,601 SqFt Residential MLS® # 1228705
New
1405 Fryston St, ST JOHNS

$989,900

1405 Fryston St, ST JOHNS

6 Beds 5 Baths 4,260 SqFt Residential MLS® # 1228836
New
730 Enrede Ln, ST AUGUSTINE

$879,500

730 Enrede Ln, ST AUGUSTINE

5 Beds 5 Baths 3,709 SqFt Residential MLS® # 1229031
New
108 Carling Dr, PONTE VEDRA

$740,000

108 Carling Dr, PONTE VEDRA

4 Beds 3 Baths 2,456 SqFt Residential MLS® # 1228521
New
69 Willow Lake Dr, ST AUGUSTINE

$590,000

69 Willow Lake Dr, ST AUGUSTINE

4 Beds 3 Baths 2,678 SqFt Residential MLS® # 1228917
New Pending
623 Saint Kitts Loop, ST AUGUSTINE

$725,000

623 Saint Kitts Loop, ST AUGUSTINE

5 Beds 4 Baths 3,165 SqFt Residential MLS® # 1228905
New
148 Narvarez Ave, ST AUGUSTINE

$475,000

148 Narvarez Ave, ST AUGUSTINE

3 Beds 3 Baths 2,033 SqFt Residential MLS® # 1228771
New
503 Arricola Ave, ST AUGUSTINE

$799,000

503 Arricola Ave, ST AUGUSTINE

3 Beds 3 Baths 1,908 SqFt Residential MLS® # 1228437
New Pending
353 Storybrook Point, PONTE VEDRA

$1,144,725

353 Storybrook Point, PONTE VEDRA

4 Beds 4 Baths 3,550 SqFt Residential MLS® # 1228682
2948 Las Calinas Blvd, ST AUGUSTINE

$785,000

2948 Las Calinas Blvd, ST AUGUSTINE

5 Beds 4 Baths 3,202 SqFt Residential MLS® # 1228342
Pending
308 S Checkerberry Way, ST JOHNS

$749,700

308 S Checkerberry Way, ST JOHNS

5 Beds 4 Baths 3,307 SqFt Residential MLS® # 1228098
217a S Roscoe Blvd, PONTE VEDRA BEACH

$5,999,995

217a S Roscoe Blvd, PONTE VEDRA BEACH

7 Beds 7 Baths 5,500 SqFt Residential MLS® # 1227849
70 Weeden St, ST AUGUSTINE

$875,000

70 Weeden St, ST AUGUSTINE

2 Beds 2 Baths 1,443 SqFt Residential MLS® # 1227709
Pending
520 Latrobe Ave, ST AUGUSTINE

$1,200,000

520 Latrobe Ave, ST AUGUSTINE

5 Beds 3 Baths 3,483 SqFt Residential MLS® # 1225836
Under Contract
547 Captiva Dr, PONTE VEDRA

$699,900

547 Captiva Dr, PONTE VEDRA

4 Beds 4 Baths 2,715 SqFt Residential MLS® # 1227479
5012 Blackhawk Dr, ST JOHNS

$850,000

↓ $25,000

5012 Blackhawk Dr, ST JOHNS

5 Beds 5 Baths 3,409 SqFt Residential MLS® # 1225363
67 Callisto Way, ST JOHNS

$898,000

↓ $31,000

67 Callisto Way, ST JOHNS

4 Beds 5 Baths 3,851 SqFt Residential MLS® # 1227138
New
1175 Eastwood Branch Dr, JACKSONVILLE

$787,000

1175 Eastwood Branch Dr, JACKSONVILLE

5 Beds 4 Baths 3,402 SqFt Residential MLS® # 1227050
467 Royal Tern Rd S, PONTE VEDRA BEACH

$3,295,000

467 Royal Tern Rd S, PONTE VEDRA BEACH

5 Beds 6 Baths 6,130 SqFt Residential MLS® # 1226425
New
129 Havencrest Ave, PONTE VEDRA

$619,000

129 Havencrest Ave, PONTE VEDRA

2 Beds 2 Baths 1,591 SqFt Residential MLS® # 1226970

St. John's County Homes With Guest Suite Market Data

St. John's County Homes With Guest Suite housing market statistics: As of May 29, 2023 there are currently 153 properties for sale in St. John's County Homes With Guest Suite, with an average asking price of $1,244,440. The highest-priced property is $8,500,000 and the lowest-priced property can be purchased for $475,000. St. John's County Homes With Guest Suite listings have an average price of $347 per square feet, based on listings with 4 beds, 4 baths, and 3,390 square feet of living space.