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

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New
410 Tanager Road, St. Augustine

$414,900

410 Tanager Road, St. Augustine

3 Beds 2 Baths 1,028 SqFt Residential MLS® # 2112205
New
114 Logrono Court, St. Augustine

$435,000

114 Logrono Court, St. Augustine

4 Beds 3 Baths 2,491 SqFt Residential MLS® # 2112789
New
632 Battersea Drive, St. Augustine

$779,000

632 Battersea Drive, St. Augustine

4 Beds 4 Baths 2,882 SqFt Residential MLS® # 2113173
New
210 Goya Way, St. Augustine

$499,990

210 Goya Way, St. Augustine

4 Beds 2 Baths 2,336 SqFt Residential MLS® # 2113147
New
382 Higgins Loop, St. Augustine

$645,165

382 Higgins Loop, St. Augustine

5 Beds 5 Baths 3,381 SqFt Residential MLS® # 2113128
New
95 Bellaire, St. Augustine

$579,475

95 Bellaire, St. Augustine

4 Beds 3 Baths 2,657 SqFt Residential MLS® # 2113123
New
591 Julia Street, St. Augustine

$275,000

591 Julia Street, St. Augustine

3 Beds 1 Bath 916 SqFt Residential MLS® # 2113114
New
207 Merchant Avenue, St. Johns

$667,382

207 Merchant Avenue, St. Johns

3 Beds 3 Baths 2,506 SqFt Residential MLS® # 2113092
New
210 Appalachian Trail, St. Johns

$447,415

210 Appalachian Trail, St. Johns

3 Beds 2 Baths 1,738 SqFt Residential MLS® # 2113088
New
207 Appalachian Trail, St. Johns

$412,144

207 Appalachian Trail, St. Johns

3 Beds 2 Baths 1,367 SqFt Residential MLS® # 2113081
145 Deer Haven Drive, Ponte Vedra Beach

$1,599,000

145 Deer Haven Drive, Ponte Vedra Beach

4 Beds 4 Baths 3,889 SqFt Residential MLS® # 2092231
191 Bluegrass Way, St. Augustine

$379,990

191 Bluegrass Way, St. Augustine

3 Beds 2 Baths 1,622 SqFt Residential MLS® # 2081273
New
261 Sand Harbor Drive, Ponte Vedra

$775,000

261 Sand Harbor Drive, Ponte Vedra

3 Beds 4 Baths 2,761 SqFt Residential MLS® # 2113046
New
416 Ocean Grove Circle Circle, St. Augustine

$1,695,000

416 Ocean Grove Circle Circle, St. Augustine

5 Beds 4 Baths 3,369 SqFt Residential MLS® # 2113039
New
362 Cedarstone Way, St. Augustine

$755,000

362 Cedarstone Way, St. Augustine

4 Beds 4 Baths 2,796 SqFt Residential MLS® # 2113036
New
249 Pasarela Drive, St. Augustine

$1,350,000

249 Pasarela Drive, St. Augustine

4 Beds 3 Baths 3,166 SqFt Residential MLS® # 2113033
922 Brook Forest Drive, St. Augustine

$524,990

922 Brook Forest Drive, St. Augustine

5 Beds 3 Baths 2,289 SqFt Residential MLS® # 2081116
New
958 Pantano Drive, St. Augustine

$1,189,000

958 Pantano Drive, St. Augustine

4 Beds 5 Baths 4,055 SqFt Residential MLS® # 2113008
New
1006 Pantano Drive, St. Augustine

$1,021,000

↑ $89,000

1006 Pantano Drive, St. Augustine

4 Beds 5 Baths 2,987 SqFt Residential MLS® # 2113006
New
180 Pelican Pointe Road, Ponte Vedra

$750,000

180 Pelican Pointe Road, Ponte Vedra

4 Beds 3 Baths 2,789 SqFt Residential MLS® # 2081319
8435 Florence Cove Road, St. Augustine

$680,000

8435 Florence Cove Road, St. Augustine

3 Beds 2 Baths 1,872 SqFt Residential MLS® # 2086046
New
1450 Wentworth Avenue, St. Johns

$1,599,500

1450 Wentworth Avenue, St. Johns

6 Beds 7 Baths 7,308 SqFt Residential MLS® # 2043467
New Pending
577 Knotted Birch Avenue, St. Augustine

$780,990

577 Knotted Birch Avenue, St. Augustine

2 Beds 2 Baths 3,129 SqFt Residential MLS® # 2112994
New Pending
624 Knotted Birch Avenue, St. Augustine

$780,990

624 Knotted Birch Avenue, St. Augustine

2 Beds 2 Baths 3,129 SqFt Residential MLS® # 2112993

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

St. John's County Homes With Guest Suite housing market statistics: As of October 14, 2025 there are currently 2,478 properties for sale in St. John's County Homes With Guest Suite, with an average asking price of $844,627. The highest-priced property is $21,250,000 and the lowest-priced property can be purchased for $179,900. St. John's County Homes With Guest Suite listings have an average price of $310 per square feet, based on listings with 4 beds, 3 baths, and 2,533 square feet of living space.