diff --git a/cli/tests/integration/secret_store.rs b/cli/tests/integration/secret_store.rs
index 25ef674a..dbc911ed 100644
--- a/cli/tests/integration/secret_store.rs
+++ b/cli/tests/integration/secret_store.rs
@@ -14,6 +14,7 @@ viceroy_test!(secret_store_works, |is_component| {
         language = "rust"
         [local_server]
         secret_stores.store_one = [{key = "first", data = "This is some data"},{key = "second", file = "../test-fixtures/data/kv-store.txt"}]
+        secret_stores.store_two = {file = "../test-fixtures/data/json-secret_store.json", format = "json"}
     "#;
 
     let resp = Test::using_fixture("secret-store.wasm")
diff --git a/lib/src/config/secret_store.rs b/lib/src/config/secret_store.rs
index 28c00b29..e2395ac5 100644
--- a/lib/src/config/secret_store.rs
+++ b/lib/src/config/secret_store.rs
@@ -3,7 +3,7 @@ use {
         error::{FastlyConfigError, SecretStoreConfigError},
         secret_store::{SecretStore, SecretStores},
     },
-    std::{convert::TryFrom, fs},
+    std::{collections::HashMap, convert::TryFrom, fs},
     toml::value::Table,
 };
 
@@ -23,12 +23,66 @@ impl TryFrom<Table> for SecretStoreConfig {
                 });
             }
 
-            let items = items.as_array().ok_or_else(|| {
-                FastlyConfigError::InvalidSecretStoreDefinition {
-                    name: store_name.to_string(),
-                    err: SecretStoreConfigError::NotAnArray,
+            // Either the items here is from a top-level file with
+            // "file" and "format" keys or it's an inline array.
+            // We try to parse either one of them to the same Vec<toml::Value>
+            // to allow them to run through the same validation path futher down
+            let file_path = items
+                .as_table()
+                .and_then(|table| table.get("file"))
+                .and_then(|file| file.as_str());
+            let file_format = items
+                .as_table()
+                .and_then(|table| table.get("format"))
+                .and_then(|format| format.as_str());
+
+            let items: Vec<toml::Value> = match (file_path, file_format) {
+                (Some(file_path), Some(file_type)) => {
+                    if file_type != "json" {
+                        return Err(FastlyConfigError::InvalidSecretStoreDefinition {
+                            name: store_name.to_string(),
+                            err: SecretStoreConfigError::InvalidFileFormat(file_type.to_string()),
+                        });
+                    }
+
+                    let json = read_json_contents(&file_path).map_err(|e| {
+                        FastlyConfigError::InvalidSecretStoreDefinition {
+                            name: store_name.to_string(),
+                            err: e,
+                        }
+                    })?;
+
+                    let toml: Vec<toml::Value> = json
+                        .into_iter()
+                        .map(|(key, value)| {
+                            toml::toml! {
+                                key = key
+                                data = value
+                            }
+                        })
+                        .collect();
+
+                    toml
+                }
+                (None, None) => {
+                    // No file or format specified, parse the TOML as an array
+                    items
+                        .as_array()
+                        .ok_or_else(|| FastlyConfigError::InvalidSecretStoreDefinition {
+                            name: store_name.to_string(),
+                            err: SecretStoreConfigError::NotAnArray,
+                        })?
+                        .clone()
                 }
-            })?;
+                // This means that *either* `format` or `file` is set, which isn't allowed
+                // we need both or neither.
+                (_, _) => {
+                    return Err(FastlyConfigError::InvalidSecretStoreDefinition {
+                        name: store_name.to_string(),
+                        err: SecretStoreConfigError::OnlyOneFormatOrFileSet,
+                    });
+                }
+            };
 
             let mut secret_store = SecretStore::new();
             for item in items.iter() {
@@ -112,3 +166,10 @@ fn is_valid_name(name: &str) -> bool {
             .chars()
             .all(|c| c.is_ascii_alphanumeric() || c == '_' || c == '-' || c == '.')
 }
+
+fn read_json_contents(filename: &str) -> Result<HashMap<String, String>, SecretStoreConfigError> {
+    let data = fs::read_to_string(filename).map_err(SecretStoreConfigError::IoError)?;
+    let map: HashMap<String, String> =
+        serde_json::from_str(&data).map_err(|_| SecretStoreConfigError::FileWrongFormat)?;
+    Ok(map)
+}
diff --git a/lib/src/error.rs b/lib/src/error.rs
index b6ff8538..765399a8 100644
--- a/lib/src/error.rs
+++ b/lib/src/error.rs
@@ -666,6 +666,14 @@ pub enum SecretStoreConfigError {
     #[error(transparent)]
     IoError(std::io::Error),
 
+    #[error("'{0}' is not a valid format for the secret store. Supported format(s) are: 'json'.")]
+    InvalidFileFormat(String),
+    #[error("When using a top-level 'file' to load data, both 'file' and 'format' must be set.")]
+    OnlyOneFormatOrFileSet,
+    #[error(
+        "The file is of the wrong format. The file is expected to contain a single JSON object."
+    )]
+    FileWrongFormat,
     #[error("The `file` and `data` keys for the object `{0}` are set. Only one can be used.")]
     FileAndData(String),
     #[error("The `file` or `data` key for the object `{0}` is not set. One must be used.")]
diff --git a/test-fixtures/data/json-secret_store.json b/test-fixtures/data/json-secret_store.json
new file mode 100644
index 00000000..c62326c1
--- /dev/null
+++ b/test-fixtures/data/json-secret_store.json
@@ -0,0 +1,4 @@
+{
+    "first": "first secret",
+    "second": "another secret"
+}
diff --git a/test-fixtures/src/bin/secret-store.rs b/test-fixtures/src/bin/secret-store.rs
index 33644fd8..f8771fe0 100644
--- a/test-fixtures/src/bin/secret-store.rs
+++ b/test-fixtures/src/bin/secret-store.rs
@@ -22,6 +22,13 @@ fn main() {
         _ => panic!(),
     }
 
+    let store_two = SecretStore::open("store_two").unwrap();
+    assert_eq!(store_two.get("first").unwrap().plaintext(), "first secret");
+    assert_eq!(
+        store_two.get("second").unwrap().plaintext(),
+        "another secret",
+    );
+
     let hello_bytes = "hello, wasm_world!".as_bytes().to_vec();
     let secret = Secret::from_bytes(hello_bytes).unwrap();
     assert_eq!("hello, wasm_world!", secret.plaintext());