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

Sort by:
New
136 Strong Branch Drive, Ponte Vedra Beach

$1,399,000

136 Strong Branch Drive, Ponte Vedra Beach

4 Beds 4 Baths 3,241 SqFt Residential MLS® # 2098311
New
112 Findhorn Court, St. Johns

$442,000

112 Findhorn Court, St. Johns

3 Beds 2 Baths 1,966 SqFt Residential MLS® # 2098303
New
4385 Comanche Trail Boulevard, St. Johns

$385,000

4385 Comanche Trail Boulevard, St. Johns

3 Beds 2 Baths 1,418 SqFt Residential MLS® # 2098300
New
100 Adela Street, St. Augustine

$489,900

100 Adela Street, St. Augustine

3 Beds 2 Baths 1,885 SqFt Residential MLS® # 2098295
New
8961 Jimmy Buffett Mem Highway, St. Augustine

$679,000

8961 Jimmy Buffett Mem Highway, St. Augustine

4 Beds 3 Baths 2,304 SqFt Residential MLS® # 2098291
New
720 Toria Lane, St. Augustine

$675,000

720 Toria Lane, St. Augustine

4 Beds 3 Baths 2,567 SqFt Residential MLS® # 2097330
New
313 Caminha Road, St. Augustine

$375,000

313 Caminha Road, St. Augustine

4 Beds 2 Baths 1,774 SqFt Residential MLS® # 2098244
New
2545 S Ponte Vedra Boulevard, Ponte Vedra Beach

$2,885,000

2545 S Ponte Vedra Boulevard, Ponte Vedra Beach

4 Beds 3 Baths 3,751 SqFt Residential MLS® # 2026353
New
126 Tabby Lake Avenue, St. Augustine

$524,900

126 Tabby Lake Avenue, St. Augustine

4 Beds 3 Baths 2,253 SqFt Residential MLS® # 2098237
New
121 Seamount Way, St. Augustine

$725,000

121 Seamount Way, St. Augustine

4 Beds 3 Baths 3,000 SqFt Residential MLS® # 2098228
New
243 Ravenswood Drive, St. Augustine

$314,000

243 Ravenswood Drive, St. Augustine

3 Beds 2 Baths 1,056 SqFt Residential MLS® # 2098224
New
269 S Matanzas Boulevard, St. Augustine

$1,500,000

269 S Matanzas Boulevard, St. Augustine

5 Beds 4 Baths 3,495 SqFt Residential MLS® # 1228553
New
2614 St Noelle Court S, Ponte Vedra Beach

$499,000

2614 St Noelle Court S, Ponte Vedra Beach

3 Beds 2 Baths 1,283 SqFt Residential MLS® # 2098209
New
303 Gulfstream Way, Ponte Vedra

$1,099,999

303 Gulfstream Way, Ponte Vedra

4 Beds 3 Baths 3,223 SqFt Residential MLS® # 2098185
New
148 Ancient Island Drive, St. Augustine

$659,000

148 Ancient Island Drive, St. Augustine

4 Beds 3 Baths 2,495 SqFt Residential MLS® # 2098160
New
157 Heron Landing Road, St. Johns

$510,000

157 Heron Landing Road, St. Johns

3 Beds 3 Baths 2,366 SqFt Residential MLS® # 2098155
New
24736 Harbour View Drive, Ponte Vedra Beach

$5,195,000

24736 Harbour View Drive, Ponte Vedra Beach

6 Beds 9 Baths 9,122 SqFt Residential MLS® # 2097107
New Pending
581 Kingbird Drive, St. Augustine

$506,480

581 Kingbird Drive, St. Augustine

4 Beds 2 Baths 2,106 SqFt Residential MLS® # 2098134
New Pending
122 Bluegrass Way, St. Augustine

$445,480

122 Bluegrass Way, St. Augustine

4 Beds 3 Baths 1,943 SqFt Residential MLS® # 2098130
New
416 Friar Tuck Lane, St. Augustine

$1,090,000

416 Friar Tuck Lane, St. Augustine

4 Beds 3 Baths 2,442 SqFt Residential MLS® # 2098131
New Pending
68 Bluegrass Way, St. Augustine

$409,990

68 Bluegrass Way, St. Augustine

4 Beds 3 Baths 1,943 SqFt Residential MLS® # 2098129
New Pending
170 Hasler Avenue, St. Augustine

$652,980

170 Hasler Avenue, St. Augustine

5 Beds 4 Baths 3,381 SqFt Residential MLS® # 2098125
New Pending
436 Hasler Avenue, St. Augustine

$496,980

436 Hasler Avenue, St. Augustine

4 Beds 3 Baths 2,028 SqFt Residential MLS® # 2098123
New
110 Abalone Lane W, Ponte Vedra Beach

$525,000

110 Abalone Lane W, Ponte Vedra Beach

3 Beds 2 Baths 1,466 SqFt Residential MLS® # 2098116

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

St. John's County Homes With Guest Suite housing market statistics: As of July 12, 2025 there are currently 2,933 properties for sale in St. John's County Homes With Guest Suite, with an average asking price of $858,494. The highest-priced property is $21,250,000 and the lowest-priced property can be purchased for $110,000. St. John's County Homes With Guest Suite listings have an average price of $318 per square feet, based on listings with 4 beds, 3 baths, and 2,542 square feet of living space.