diff --git a/CHANGELOG.md b/CHANGELOG.md
index 3fc971af41..028bfc3ab3 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -2,14 +2,12 @@
 
 # UNRELEASED
 
-## Dependencies
-
-## Fixes
-
 ### fix: correct `dfx sns` example commands in documentation
 
 Fixed incorrect commands `dfx sns config create` and `dfx sns config validate` in the `dfx sns` CLI reference examples. The correct commands are `dfx sns create` and `dfx sns validate`.
 
+### fix: Failure to query an asset canister's API version no longer gets misinterpreted as the canister being outdated
+
 ### Motoko
 
 Updated Motoko to [1.2.0](https://github.com/dfinity/motoko/releases/tag/1.2.0)
diff --git a/src/canisters/frontend/ic-asset/src/canister_api/methods/api_version.rs b/src/canisters/frontend/ic-asset/src/canister_api/methods/api_version.rs
index 1c9a139a86..81396992b4 100644
--- a/src/canisters/frontend/ic-asset/src/canister_api/methods/api_version.rs
+++ b/src/canisters/frontend/ic-asset/src/canister_api/methods/api_version.rs
@@ -1,12 +1,25 @@
 use crate::canister_api::methods::method_names::API_VERSION;
+use ic_agent::AgentError;
 use ic_utils::Canister;
 use ic_utils::call::SyncCall;
 
-pub(crate) async fn api_version(canister: &Canister<'_>) -> u16 {
-    canister
-        .query(API_VERSION)
-        .build()
-        .call()
-        .await
-        .map_or(0, |v: (u16,)| v.0)
+const CANISTER_METHOD_NOT_FOUND: &str = "IC0536";
+
+fn is_method_not_found(err: &AgentError) -> bool {
+    match err {
+        AgentError::CertifiedReject { reject, .. }
+        | AgentError::UncertifiedReject { reject, .. } => {
+            reject.error_code.as_deref() == Some(CANISTER_METHOD_NOT_FOUND)
+        }
+        _ => false,
+    }
+}
+
+pub(crate) async fn api_version(canister: &Canister<'_>) -> Result<u16, AgentError> {
+    match canister.query(API_VERSION).build().call().await {
+        Ok((version,)) => Ok(version),
+        // If the canister doesn't have the `api_version` method, it's an old version of the API.
+        Err(e) if is_method_not_found(&e) => Ok(0),
+        Err(e) => Err(e),
+    }
 }
diff --git a/src/canisters/frontend/ic-asset/src/error/prepare_sync_for_proposal.rs b/src/canisters/frontend/ic-asset/src/error/prepare_sync_for_proposal.rs
index a22a5dd871..8886cc4488 100644
--- a/src/canisters/frontend/ic-asset/src/error/prepare_sync_for_proposal.rs
+++ b/src/canisters/frontend/ic-asset/src/error/prepare_sync_for_proposal.rs
@@ -5,6 +5,10 @@ use thiserror::Error;
 /// Errors related to preparing synchronization operations for a proposal.
 #[derive(Error, Debug)]
 pub enum PrepareSyncForProposalError {
+    /// Failed when querying the asset canister for its API version.
+    #[error("Failed to query asset canister API version")]
+    ApiVersionQueryFailed(#[source] AgentError),
+
     /// Failed while requesting that the asset canister compute evidence.
     #[error("Failed to compute evidence")]
     ComputeEvidence(#[source] AgentError),
diff --git a/src/canisters/frontend/ic-asset/src/error/sync.rs b/src/canisters/frontend/ic-asset/src/error/sync.rs
index b93f0d251c..104f7f8b89 100644
--- a/src/canisters/frontend/ic-asset/src/error/sync.rs
+++ b/src/canisters/frontend/ic-asset/src/error/sync.rs
@@ -6,6 +6,10 @@ use thiserror::Error;
 /// Errors related to the sync process.
 #[derive(Error, Debug)]
 pub enum SyncError {
+    /// Failed when querying the asset canister for its API version.
+    #[error("Failed to query asset canister API version")]
+    ApiVersionQueryFailed(#[source] AgentError),
+
     /// Failed when calling commit_batch
     #[error("Failed to commit batch")]
     CommitBatchFailed(#[source] AgentError),
diff --git a/src/canisters/frontend/ic-asset/src/error/upload.rs b/src/canisters/frontend/ic-asset/src/error/upload.rs
index d9277c483c..f085bdda64 100644
--- a/src/canisters/frontend/ic-asset/src/error/upload.rs
+++ b/src/canisters/frontend/ic-asset/src/error/upload.rs
@@ -7,6 +7,10 @@ use thiserror::Error;
 /// Errors encountered during the upload process.
 #[derive(Error, Debug)]
 pub enum UploadError {
+    /// Failed when querying the asset canister for its API version.
+    #[error("Failed to query asset canister API version")]
+    ApiVersionQueryFailed(#[source] AgentError),
+
     /// Failed when calling commit_batch.
     #[error("Commit batch failed")]
     CommitBatchFailed(#[source] AgentError),
diff --git a/src/canisters/frontend/ic-asset/src/sync.rs b/src/canisters/frontend/ic-asset/src/sync.rs
index 521719e4a2..76e5b0b95d 100644
--- a/src/canisters/frontend/ic-asset/src/sync.rs
+++ b/src/canisters/frontend/ic-asset/src/sync.rs
@@ -28,7 +28,7 @@ use crate::error::GatherAssetDescriptorsError::{
 };
 use crate::error::PrepareSyncForProposalError;
 use crate::error::SyncError;
-use crate::error::SyncError::CommitBatchFailed;
+use crate::error::SyncError::{ApiVersionQueryFailed, CommitBatchFailed};
 use crate::error::UploadContentError;
 use crate::error::UploadContentError::{CreateBatchFailed, ListAssetsFailed};
 use crate::progress::{AssetSyncProgressRenderer, AssetSyncState};
@@ -155,7 +155,7 @@ pub async fn sync(
     logger: &Logger,
     progress: Option<&dyn AssetSyncProgressRenderer>,
 ) -> Result<(), SyncError> {
-    let canister_api_version = api_version(canister).await;
+    let canister_api_version = api_version(canister).await.map_err(ApiVersionQueryFailed)?;
     let commit_batch_args = upload_content_and_assemble_sync_operations(
         canister,
         canister_api_version,
@@ -296,7 +296,9 @@ pub async fn prepare_sync_for_proposal(
     logger: &Logger,
     progress: Option<&dyn AssetSyncProgressRenderer>,
 ) -> Result<(Nat, ByteBuf), PrepareSyncForProposalError> {
-    let canister_api_version = api_version(canister).await;
+    let canister_api_version = api_version(canister)
+        .await
+        .map_err(PrepareSyncForProposalError::ApiVersionQueryFailed)?;
     let arg = upload_content_and_assemble_sync_operations(
         canister,
         canister_api_version,
diff --git a/src/canisters/frontend/ic-asset/src/upload.rs b/src/canisters/frontend/ic-asset/src/upload.rs
index 2db6654072..e91c637554 100644
--- a/src/canisters/frontend/ic-asset/src/upload.rs
+++ b/src/canisters/frontend/ic-asset/src/upload.rs
@@ -14,7 +14,9 @@ use crate::canister_api::methods::{
 };
 use crate::canister_api::types::batch_upload::v0;
 use crate::error::CompatibilityError::DowngradeV1TOV0Failed;
-use crate::error::UploadError::{self, CommitBatchFailed, CreateBatchFailed, ListAssetsFailed};
+use crate::error::UploadError::{
+    self, ApiVersionQueryFailed, CommitBatchFailed, CreateBatchFailed, ListAssetsFailed,
+};
 use ic_utils::Canister;
 use slog::{Logger, info};
 use std::collections::HashMap;
@@ -41,7 +43,7 @@ pub async fn upload(
     info!(logger, "Starting batch.");
 
     let batch_id = create_batch(canister).await.map_err(CreateBatchFailed)?;
-    let canister_api_version = api_version(canister).await;
+    let canister_api_version = api_version(canister).await.map_err(ApiVersionQueryFailed)?;
 
     info!(logger, "Staging contents of new and changed assets:");
 
@@ -69,7 +71,7 @@ pub async fn upload(
     .await
     .map_err(UploadError::AssembleCommitBatchArgumentFailed)?;
 
-    let canister_api_version = api_version(canister).await;
+    let canister_api_version = api_version(canister).await.map_err(ApiVersionQueryFailed)?;
     info!(logger, "Committing batch.");
     match canister_api_version {
         0 => {