diff --git a/crates/trusted-server-adapter-fastly/src/error.rs b/crates/trusted-server-adapter-fastly/src/error.rs
index 560a2e18..f3182ddc 100644
--- a/crates/trusted-server-adapter-fastly/src/error.rs
+++ b/crates/trusted-server-adapter-fastly/src/error.rs
@@ -17,3 +17,26 @@ pub fn to_error_response(report: &Report<TrustedServerError>) -> Response {
     Response::from_status(root_error.status_code())
         .with_body_text_plain(&format!("{}\n", root_error.user_message()))
 }
+
+#[cfg(test)]
+mod tests {
+    use super::*;
+
+    #[test]
+    fn config_store_unavailable_renders_503() {
+        // Locks the end-to-end mapping: a config-store read failure reaches the
+        // client as 503 via `status_code()` — not bypassed by the adapter.
+        let report = Report::new(TrustedServerError::ConfigStoreUnavailable {
+            store_name: "app_config".to_string(),
+            message: "unavailable or not seeded".to_string(),
+        });
+
+        let response = to_error_response(&report);
+
+        assert_eq!(
+            response.get_status(),
+            fastly::http::StatusCode::SERVICE_UNAVAILABLE,
+            "config-store read failure should render as 503 to the client"
+        );
+    }
+}
diff --git a/crates/trusted-server-core/src/error.rs b/crates/trusted-server-core/src/error.rs
index 2804afec..ed934bb6 100644
--- a/crates/trusted-server-core/src/error.rs
+++ b/crates/trusted-server-core/src/error.rs
@@ -26,6 +26,11 @@ pub enum TrustedServerError {
     #[display("Configuration error: {message}")]
     Configuration { message: String },
 
+    /// Config store could not be read (unseeded, transient backend, or a listed
+    /// key missing) — Settings cannot be loaded. Retryable / fix by seeding.
+    #[display("Config store unavailable: {store_name} - {message}")]
+    ConfigStoreUnavailable { store_name: String, message: String },
+
     /// Auction orchestration error.
     #[display("Auction error: {message}")]
     Auction { message: String },
@@ -123,6 +128,7 @@ impl IntoHttpResponse for TrustedServerError {
             Self::InvalidHeaderValue { .. } => StatusCode::BAD_REQUEST,
             Self::InvalidUtf8 { .. } => StatusCode::INTERNAL_SERVER_ERROR,
             Self::KvStore { .. } => StatusCode::SERVICE_UNAVAILABLE,
+            Self::ConfigStoreUnavailable { .. } => StatusCode::SERVICE_UNAVAILABLE,
             Self::Prebid { .. } => StatusCode::BAD_GATEWAY,
             Self::Integration { .. } => StatusCode::BAD_GATEWAY,
             Self::Proxy { .. } => StatusCode::BAD_GATEWAY,
@@ -211,6 +217,13 @@ mod tests {
                 },
                 StatusCode::SERVICE_UNAVAILABLE,
             ),
+            (
+                TrustedServerError::ConfigStoreUnavailable {
+                    store_name: String::from("app_config"),
+                    message: String::from("store unavailable"),
+                },
+                StatusCode::SERVICE_UNAVAILABLE,
+            ),
             (
                 TrustedServerError::Prebid {
                     message: String::from("adapter error"),
@@ -286,6 +299,9 @@ mod tests {
                 TrustedServerError::RequestTooLarge { .. } => StatusCode::PAYLOAD_TOO_LARGE,
                 TrustedServerError::InvalidHeaderValue { .. } => StatusCode::BAD_REQUEST,
                 TrustedServerError::KvStore { .. } => StatusCode::SERVICE_UNAVAILABLE,
+                TrustedServerError::ConfigStoreUnavailable { .. } => {
+                    StatusCode::SERVICE_UNAVAILABLE
+                }
                 TrustedServerError::Prebid { .. } => StatusCode::BAD_GATEWAY,
                 TrustedServerError::Integration { .. } => StatusCode::BAD_GATEWAY,
                 TrustedServerError::Proxy { .. } => StatusCode::BAD_GATEWAY,
@@ -400,6 +416,25 @@ mod tests {
         assert_eq!(error.user_message(), "Invalid header value");
     }
 
+    #[test]
+    fn config_store_unavailable_maps_to_503() {
+        let error = TrustedServerError::ConfigStoreUnavailable {
+            store_name: String::from("app_config"),
+            message: String::from("unavailable or not seeded"),
+        };
+        assert_eq!(
+            error.status_code(),
+            StatusCode::SERVICE_UNAVAILABLE,
+            "config-store read failure should map to 503"
+        );
+        // Detail stays server-side; the public body is the generic catch-all.
+        assert_eq!(
+            error.user_message(),
+            "An internal error occurred",
+            "503 client body must not leak internal config-store detail"
+        );
+    }
+
     #[test]
     fn status_code_maps_each_error_variant_to_expected_http_response() {
         // Compile-time guard: adding a TrustedServerError variant without
@@ -413,6 +448,7 @@ mod tests {
             | TrustedServerError::InvalidUtf8 { .. }
             | TrustedServerError::InvalidHeaderValue { .. }
             | TrustedServerError::KvStore { .. }
+            | TrustedServerError::ConfigStoreUnavailable { .. }
             | TrustedServerError::Prebid { .. }
             | TrustedServerError::Integration { .. }
             | TrustedServerError::Proxy { .. }
@@ -499,6 +535,13 @@ mod tests {
                 },
                 StatusCode::SERVICE_UNAVAILABLE,
             ),
+            (
+                TrustedServerError::ConfigStoreUnavailable {
+                    store_name: "app_config".to_string(),
+                    message: "config store unavailable".to_string(),
+                },
+                StatusCode::SERVICE_UNAVAILABLE,
+            ),
             (
                 TrustedServerError::Auction {
                     message: "auction failed".to_string(),
diff --git a/crates/trusted-server-core/src/settings_data.rs b/crates/trusted-server-core/src/settings_data.rs
index bdf46a84..4ad7c9b1 100644
--- a/crates/trusted-server-core/src/settings_data.rs
+++ b/crates/trusted-server-core/src/settings_data.rs
@@ -36,9 +36,12 @@ struct FastlyChunkRef {
 ///
 /// # Errors
 ///
-/// Returns [`TrustedServerError::Configuration`] when the config blob is
-/// missing, cannot be read, fails envelope verification, or fails Trusted
-/// Server settings validation.
+/// Returns [`TrustedServerError::ConfigStoreUnavailable`] (HTTP 503) when the
+/// config blob (or a referenced chunk) cannot be read — store unseeded,
+/// transient backend, or a chunk key missing. Returns
+/// [`TrustedServerError::Configuration`] (HTTP 500) when the read succeeds but
+/// the blob fails envelope/chunk verification or Trusted Server settings
+/// validation.
 pub fn get_settings_from_services(
     services: &RuntimeServices,
 ) -> Result<Settings, Report<TrustedServerError>> {
@@ -66,9 +69,10 @@ pub fn default_config_key() -> String {
 ///
 /// # Errors
 ///
-/// Returns [`TrustedServerError::Configuration`] when the config blob is
-/// missing, cannot be read, fails envelope verification, or fails Trusted
-/// Server settings validation.
+/// Returns [`TrustedServerError::ConfigStoreUnavailable`] (HTTP 503) when the
+/// config blob (or a referenced chunk) cannot be read, and
+/// [`TrustedServerError::Configuration`] (HTTP 500) when the read succeeds but
+/// envelope/chunk verification or settings validation fails.
 pub fn get_settings_from_config_store(
     config_store: &dyn PlatformConfigStore,
     store_name: &StoreName,
@@ -84,12 +88,14 @@ fn read_config_entry(
     store_name: &StoreName,
     key: &str,
 ) -> Result<String, Report<TrustedServerError>> {
-    let message = format!(
-        "failed to read Trusted Server app config key `{key}` from config store `{store_name}`"
-    );
     config_store
         .get(store_name, key)
-        .change_context(TrustedServerError::Configuration { message })
+        .change_context(TrustedServerError::ConfigStoreUnavailable {
+            store_name: store_name.to_string(),
+            message: format!(
+                "unavailable or not seeded (failed to read `{key}`) — run `ts config push`"
+            ),
+        })
 }
 
 fn resolve_fastly_chunk_pointer(
@@ -160,6 +166,7 @@ fn configuration_error<T>(message: String) -> Result<T, Report<TrustedServerErro
 mod tests {
     use super::*;
     use crate::config_payload::CONFIG_BLOB_KEY;
+    use crate::error::IntoHttpResponse;
     use crate::platform::PlatformError;
     use crate::settings::Settings;
     use crate::test_support::tests::crate_test_settings_str;
@@ -269,7 +276,7 @@ mod tests {
     }
 
     #[test]
-    fn fails_when_blob_key_is_missing() {
+    fn unseeded_blob_is_config_store_unavailable_503() {
         let store = MemoryConfigStore {
             entries: BTreeMap::new(),
         };
@@ -278,9 +285,124 @@ mod tests {
             get_settings_from_config_store(&store, &StoreName::from("app_config"), CONFIG_BLOB_KEY)
                 .expect_err("should fail when blob is missing");
 
+        // Unseeded store is a read failure → 503, not an opaque 500.
+        assert_eq!(
+            err.current_context().status_code(),
+            http::StatusCode::SERVICE_UNAVAILABLE,
+            "unseeded config blob should map to 503"
+        );
+        // The actionable hint must ride the error chain so it reaches the
+        // server log; the public 503 body stays generic by design.
         assert!(
-            err.to_string().contains(CONFIG_BLOB_KEY),
-            "error should mention missing blob key"
+            format!("{err:?}").contains("ts config push"),
+            "error chain should carry the actionable `ts config push` hint for logs"
+        );
+    }
+
+    #[test]
+    fn missing_chunk_is_config_store_unavailable_503() {
+        // The blob key resolves to a chunk pointer, but one referenced chunk is
+        // absent — still a config-store read failure → 503.
+        let settings =
+            Settings::from_toml(&crate_test_settings_str()).expect("should parse test settings");
+        let envelope_json = envelope_json(&settings);
+        let midpoint = envelope_json.len() / 2;
+        let first_chunk = envelope_json[..midpoint].to_string();
+        let second_chunk = envelope_json[midpoint..].to_string();
+        let first_key = format!("{CONFIG_BLOB_KEY}.__edgezero_chunks.test.0");
+        let second_key = format!("{CONFIG_BLOB_KEY}.__edgezero_chunks.test.1");
+        let pointer = json!({
+            "edgezero_kind": FASTLY_CHUNK_POINTER_KIND,
+            "version": 1,
+            "envelope_sha256": sha256_hex(envelope_json.as_bytes()),
+            "envelope_len": envelope_json.len(),
+            "chunks": [
+                { "key": first_key, "sha256": sha256_hex(first_chunk.as_bytes()), "len": first_chunk.len() },
+                { "key": second_key, "sha256": sha256_hex(second_chunk.as_bytes()), "len": second_chunk.len() }
+            ]
+        })
+        .to_string();
+        // Seed the pointer + the first chunk only; the second chunk is missing.
+        let store = MemoryConfigStore {
+            entries: BTreeMap::from([
+                (CONFIG_BLOB_KEY.to_string(), pointer),
+                (first_key, first_chunk),
+            ]),
+        };
+
+        let err =
+            get_settings_from_config_store(&store, &StoreName::from("app_config"), CONFIG_BLOB_KEY)
+                .expect_err("missing chunk must error");
+
+        assert_eq!(
+            err.current_context().status_code(),
+            http::StatusCode::SERVICE_UNAVAILABLE,
+            "a referenced chunk missing is a read failure → 503"
+        );
+    }
+
+    #[test]
+    fn malformed_blob_stays_500() {
+        // The blob key reads fine (not a chunk pointer), but its contents are not
+        // a valid envelope — reconstruct/verify failure → 500, not 503.
+        let store = MemoryConfigStore {
+            entries: BTreeMap::from([(
+                CONFIG_BLOB_KEY.to_string(),
+                "not a valid blob envelope".to_string(),
+            )]),
+        };
+
+        let err =
+            get_settings_from_config_store(&store, &StoreName::from("app_config"), CONFIG_BLOB_KEY)
+                .expect_err("malformed blob must error");
+
+        assert_eq!(
+            err.current_context().status_code(),
+            http::StatusCode::INTERNAL_SERVER_ERROR,
+            "read-OK-but-invalid blob should stay 500"
+        );
+    }
+
+    #[test]
+    fn chunk_verification_failure_stays_500() {
+        // Pointer + chunks all read successfully, but a chunk's bytes no longer
+        // match the recorded length/sha — reconstruct/verify failure → 500.
+        let settings =
+            Settings::from_toml(&crate_test_settings_str()).expect("should parse test settings");
+        let envelope_json = envelope_json(&settings);
+        let midpoint = envelope_json.len() / 2;
+        let first_chunk = envelope_json[..midpoint].to_string();
+        let second_chunk = envelope_json[midpoint..].to_string();
+        let first_key = format!("{CONFIG_BLOB_KEY}.__edgezero_chunks.test.0");
+        let second_key = format!("{CONFIG_BLOB_KEY}.__edgezero_chunks.test.1");
+        let pointer = json!({
+            "edgezero_kind": FASTLY_CHUNK_POINTER_KIND,
+            "version": 1,
+            "envelope_sha256": sha256_hex(envelope_json.as_bytes()),
+            "envelope_len": envelope_json.len(),
+            "chunks": [
+                { "key": first_key, "sha256": sha256_hex(first_chunk.as_bytes()), "len": first_chunk.len() },
+                { "key": second_key, "sha256": sha256_hex(second_chunk.as_bytes()), "len": second_chunk.len() }
+            ]
+        })
+        .to_string();
+        // Store a corrupted second chunk: reads OK, but fails length/sha checks.
+        let store = MemoryConfigStore {
+            entries: BTreeMap::from([
+                (CONFIG_BLOB_KEY.to_string(), pointer),
+                (first_key, first_chunk),
+                (second_key, "corrupted chunk bytes".to_string()),
+            ]),
+        };
+
+        let err =
+            get_settings_from_config_store(&store, &StoreName::from("app_config"), CONFIG_BLOB_KEY)
+                .expect_err("corrupt chunk must error");
+
+        assert_eq!(
+            err.current_context().status_code(),
+            http::StatusCode::INTERNAL_SERVER_ERROR,
+            "chunk that reads but fails verification should stay 500"
         );
     }
 }
diff --git a/docs/superpowers/specs/2026-06-27-edgezero-http-config-503-design.md b/docs/superpowers/specs/2026-06-27-edgezero-http-config-503-design.md
new file mode 100644
index 00000000..2097e284
--- /dev/null
+++ b/docs/superpowers/specs/2026-06-27-edgezero-http-config-503-design.md
@@ -0,0 +1,78 @@
+# Design: HTTP-Layer Config-Store Load Hardening (503)
+
+- **Date:** 2026-06-27
+- **Author:** Prakash (HTTP-layer / runtime).
+- **Status:** implemented on `feature/edgezero-269-http` (stacked on `feature/ts-cli-audit`).
+- **Supersedes:** the earlier per-key flatten/hash variant of this design. The
+  CLI now stores Trusted Server config as a single **blob** (optionally chunked
+  for Fastly value-size limits — `config_payload::settings_from_config_blob`,
+  `settings_data::FastlyChunkPointer`), so the load path and this spec are
+  re-derived against that model.
+
+---
+
+## 1. Problem
+
+The runtime rebuilds `Settings` at boot by reading the `app_config` config
+store. Before this change every read failure — including an **unseeded** store —
+mapped to `TrustedServerError::Configuration` → **500**, indistinguishable from a
+genuine code bug. `trusted-server.toml` is deleted, so an unseeded store is an
+expected operational state (fresh install, or cutover before `ts config push`),
+not a bug.
+
+## 2. Load sequence (blob model)
+
+`crates/trusted-server-core/src/settings_data.rs`:
+
+```
+get_settings_from_services
+  → get_settings_from_config_store(store, name, key)
+      → read_config_entry(key)                     // READ  — the blob value
+      → resolve_fastly_chunk_pointer(value)        // if a chunk pointer:
+          → read_config_entry(chunk.key) × N       // READ  — each chunk
+          → verify chunk len + sha, envelope len + sha   // VERIFY
+      → settings_from_config_blob(envelope_json)   // VERIFY — parse + validate
+```
+
+`read_config_entry` is the **single read seam** (used for both the top-level
+blob key and every chunk key). `key` resolves via
+`EnvConfig::store_key("config", "app_config")`.
+
+## 3. Behavior matrix (the contract)
+
+The boundary is **"couldn't read the config"** vs **"read it but it's
+invalid"** — classified by **call site**, because `PlatformConfigStore::get`
+collapses key-absent and transport failure into one `Err` (see §5).
+
+| Situation                                                                                            | Where                                 | Status                                                                     |
+| ---------------------------------------------------------------------------------------------------- | ------------------------------------- | -------------------------------------------------------------------------- |
+| Blob key or a referenced chunk cannot be read (store unseeded, transient backend, chunk key missing) | `read_config_entry`                   | **503** `ConfigStoreUnavailable`, actionable hint `run \`ts config push\`` |
+| Chunk len/sha mismatch, envelope len/sha mismatch, unsupported pointer version                       | `resolve_fastly_chunk_pointer` verify | **500** `Configuration`                                                    |
+| Blob read OK but not a valid envelope / settings invalid                                             | `settings_from_config_blob`           | **500** `Configuration`                                                    |
+| Seeded + valid                                                                                       | —                                     | `Settings` loads                                                           |
+
+503 is correct for the read column: unseeded → seed it; transient → retry.
+
+## 4. Mechanism (one new variant)
+
+`TrustedServerError::ConfigStoreUnavailable { store_name, message }` →
+`StatusCode::SERVICE_UNAVAILABLE` (precedent: the existing `KvStore` 503 arm).
+Only `read_config_entry`'s `change_context` target changes from `Configuration`
+to the new variant; all verify/parse paths are untouched. No `PlatformError`
+or `PlatformConfigStore` change.
+
+**Security:** the actionable hint rides the error chain (`Display`) to the
+**server log** only. The public 503 body stays the generic
+`user_message()` catch-all — no `user_message()` arm is added for this variant —
+so internal tooling/paths never leak to clients.
+
+## 5. Out of scope / follow-up
+
+- `PlatformConfigStore::get → Result<Option<String>>` (absence as a value, not an
+  error) would let the runtime distinguish **unseeded** (`Ok(None)`) from
+  **transient** (`Err`) precisely instead of classifying by call site. It is the
+  store-convergence direction (edgezero's own `ConfigStore::get` shape) and
+  touches every impl + caller across request-signing and DataDome — tracked as a
+  separate, cross-cutting change, not this PR.
+- Non-Fastly adapter (cloudflare/spin/axum) parity rides the EdgeZero adapter
+  stack.