diff --git a/Cargo.lock b/Cargo.lock
index dc463942ed..23c64cf0e9 100644
--- a/Cargo.lock
+++ b/Cargo.lock
@@ -2977,6 +2977,7 @@ dependencies = [
  "scopeguard",
  "serde",
  "serde_json",
+ "serde_path_to_error",
  "serde_with",
  "signal-hook",
  "smallvec",
diff --git a/Cargo.toml b/Cargo.toml
index 6df48ffc55..ab00c11dda 100644
--- a/Cargo.toml
+++ b/Cargo.toml
@@ -126,6 +126,7 @@ sd-notify = "0.4.1"
 sentry = { version = "0.31", default-features = false, features = ["backtrace", "contexts", "panic", "rustls", "reqwest" ] }
 serde = { version = "1.0", features = ["derive"] }
 serde_json = "1"
+serde_path_to_error = "0.1"
 serde_with = "2.0"
 serde_assert = "0.5.0"
 sha2 = "0.10.2"
diff --git a/libs/pageserver_api/src/models.rs b/libs/pageserver_api/src/models.rs
index c792a5eff7..60c508037e 100644
--- a/libs/pageserver_api/src/models.rs
+++ b/libs/pageserver_api/src/models.rs
@@ -314,25 +314,7 @@ impl std::ops::Deref for TenantConfigRequest {
 
 impl TenantConfigRequest {
     pub fn new(tenant_id: TenantId) -> TenantConfigRequest {
-        let config = TenantConfig {
-            checkpoint_distance: None,
-            checkpoint_timeout: None,
-            compaction_target_size: None,
-            compaction_period: None,
-            compaction_threshold: None,
-            gc_horizon: None,
-            gc_period: None,
-            image_creation_threshold: None,
-            pitr_interval: None,
-            walreceiver_connect_timeout: None,
-            lagging_wal_timeout: None,
-            max_lsn_wal_lag: None,
-            trace_read_requests: None,
-            eviction_policy: None,
-            min_resident_size_override: None,
-            evictions_low_residence_duration_metric_threshold: None,
-            gc_feedback: None,
-        };
+        let config = TenantConfig::default();
         TenantConfigRequest { tenant_id, config }
     }
 }
diff --git a/pageserver/Cargo.toml b/pageserver/Cargo.toml
index 3eb01003df..35c260740c 100644
--- a/pageserver/Cargo.toml
+++ b/pageserver/Cargo.toml
@@ -51,6 +51,7 @@ regex.workspace = true
 scopeguard.workspace = true
 serde.workspace = true
 serde_json = { workspace = true, features = ["raw_value"] }
+serde_path_to_error.workspace = true
 serde_with.workspace = true
 signal-hook.workspace = true
 smallvec = { workspace = true, features = ["write"] }
diff --git a/pageserver/src/config.rs b/pageserver/src/config.rs
index 5b170af4ef..737495d414 100644
--- a/pageserver/src/config.rs
+++ b/pageserver/src/config.rs
@@ -779,7 +779,7 @@ impl PageServerConf {
                     builder.remote_storage_config(RemoteStorageConfig::from_toml(item)?)
                 }
                 "tenant_config" => {
-                    t_conf = Self::parse_toml_tenant_conf(item)?;
+                    t_conf = TenantConfOpt::try_from(item.to_owned()).context(format!("failed to parse: '{key}'"))?;
                 }
                 "id" => builder.id(NodeId(parse_toml_u64(key, item)?)),
                 "broker_endpoint" => builder.broker_endpoint(parse_toml_string(key, item)?.parse().context("failed to parse broker endpoint")?),
@@ -853,111 +853,6 @@ impl PageServerConf {
         Ok(conf)
     }
 
-    // subroutine of parse_and_validate to parse `[tenant_conf]` section
-
-    pub fn parse_toml_tenant_conf(item: &toml_edit::Item) -> Result<TenantConfOpt> {
-        let mut t_conf: TenantConfOpt = Default::default();
-        if let Some(checkpoint_distance) = item.get("checkpoint_distance") {
-            t_conf.checkpoint_distance =
-                Some(parse_toml_u64("checkpoint_distance", checkpoint_distance)?);
-        }
-
-        if let Some(checkpoint_timeout) = item.get("checkpoint_timeout") {
-            t_conf.checkpoint_timeout = Some(parse_toml_duration(
-                "checkpoint_timeout",
-                checkpoint_timeout,
-            )?);
-        }
-
-        if let Some(compaction_target_size) = item.get("compaction_target_size") {
-            t_conf.compaction_target_size = Some(parse_toml_u64(
-                "compaction_target_size",
-                compaction_target_size,
-            )?);
-        }
-
-        if let Some(compaction_period) = item.get("compaction_period") {
-            t_conf.compaction_period =
-                Some(parse_toml_duration("compaction_period", compaction_period)?);
-        }
-
-        if let Some(compaction_threshold) = item.get("compaction_threshold") {
-            t_conf.compaction_threshold =
-                Some(parse_toml_u64("compaction_threshold", compaction_threshold)?.try_into()?);
-        }
-
-        if let Some(image_creation_threshold) = item.get("image_creation_threshold") {
-            t_conf.image_creation_threshold = Some(
-                parse_toml_u64("image_creation_threshold", image_creation_threshold)?.try_into()?,
-            );
-        }
-
-        if let Some(gc_horizon) = item.get("gc_horizon") {
-            t_conf.gc_horizon = Some(parse_toml_u64("gc_horizon", gc_horizon)?);
-        }
-
-        if let Some(gc_period) = item.get("gc_period") {
-            t_conf.gc_period = Some(parse_toml_duration("gc_period", gc_period)?);
-        }
-
-        if let Some(pitr_interval) = item.get("pitr_interval") {
-            t_conf.pitr_interval = Some(parse_toml_duration("pitr_interval", pitr_interval)?);
-        }
-        if let Some(walreceiver_connect_timeout) = item.get("walreceiver_connect_timeout") {
-            t_conf.walreceiver_connect_timeout = Some(parse_toml_duration(
-                "walreceiver_connect_timeout",
-                walreceiver_connect_timeout,
-            )?);
-        }
-        if let Some(lagging_wal_timeout) = item.get("lagging_wal_timeout") {
-            t_conf.lagging_wal_timeout = Some(parse_toml_duration(
-                "lagging_wal_timeout",
-                lagging_wal_timeout,
-            )?);
-        }
-        if let Some(max_lsn_wal_lag) = item.get("max_lsn_wal_lag") {
-            t_conf.max_lsn_wal_lag =
-                Some(deserialize_from_item("max_lsn_wal_lag", max_lsn_wal_lag)?);
-        }
-        if let Some(trace_read_requests) = item.get("trace_read_requests") {
-            t_conf.trace_read_requests =
-                Some(trace_read_requests.as_bool().with_context(|| {
-                    "configure option trace_read_requests is not a bool".to_string()
-                })?);
-        }
-
-        if let Some(eviction_policy) = item.get("eviction_policy") {
-            t_conf.eviction_policy = Some(
-                deserialize_from_item("eviction_policy", eviction_policy)
-                    .context("parse eviction_policy")?,
-            );
-        }
-
-        if let Some(item) = item.get("min_resident_size_override") {
-            t_conf.min_resident_size_override = Some(
-                deserialize_from_item("min_resident_size_override", item)
-                    .context("parse min_resident_size_override")?,
-            );
-        }
-
-        if let Some(item) = item.get("evictions_low_residence_duration_metric_threshold") {
-            t_conf.evictions_low_residence_duration_metric_threshold = Some(parse_toml_duration(
-                "evictions_low_residence_duration_metric_threshold",
-                item,
-            )?);
-        }
-
-        if let Some(gc_feedback) = item.get("gc_feedback") {
-            t_conf.gc_feedback = Some(
-                gc_feedback
-                    .as_bool()
-                    .with_context(|| "configure option gc_feedback is not a bool".to_string())?,
-            );
-        }
-
-        Ok(t_conf)
-    }
-
     #[cfg(test)]
     pub fn test_repo_dir(test_name: &str) -> Utf8PathBuf {
         Utf8PathBuf::from(format!("../tmp_check/test_{test_name}"))
@@ -1429,6 +1324,37 @@ trace_read_requests = {trace_read_requests}"#,
         Ok(())
     }
 
+    #[test]
+    fn parse_incorrect_tenant_config() -> anyhow::Result<()> {
+        let config_string = r#"
+            [tenant_config]
+            checkpoint_distance = -1 # supposed to be an u64
+        "#
+        .to_string();
+
+        let toml: Document = config_string.parse()?;
+        let item = toml.get("tenant_config").unwrap();
+        let error = TenantConfOpt::try_from(item.to_owned()).unwrap_err();
+
+        let expected_error_str = "checkpoint_distance: invalid value: integer `-1`, expected u64";
+        assert_eq!(error.to_string(), expected_error_str);
+
+        Ok(())
+    }
+
+    #[test]
+    fn parse_override_tenant_config() -> anyhow::Result<()> {
+        let config_string = r#"tenant_config={ min_resident_size_override =  400 }"#.to_string();
+
+        let toml: Document = config_string.parse()?;
+        let item = toml.get("tenant_config").unwrap();
+        let conf = TenantConfOpt::try_from(item.to_owned()).unwrap();
+
+        assert_eq!(conf.min_resident_size_override, Some(400));
+
+        Ok(())
+    }
+
     #[test]
     fn eviction_pageserver_config_parse() -> anyhow::Result<()> {
         let tempdir = tempdir()?;
diff --git a/pageserver/src/tenant.rs b/pageserver/src/tenant.rs
index fe3a5bfb79..2a63f193e3 100644
--- a/pageserver/src/tenant.rs
+++ b/pageserver/src/tenant.rs
@@ -2442,9 +2442,7 @@ impl Tenant {
             for (key, item) in deserialized.iter() {
                 match key {
                     "tenant_config" => {
-                        tenant_conf = PageServerConf::parse_toml_tenant_conf(item).with_context(|| {
-                            format!("Failed to parse config from file '{legacy_config_path}' as pageserver config")
-                        })?;
+                        tenant_conf = TenantConfOpt::try_from(item.to_owned()).context(format!("Failed to parse config from file '{legacy_config_path}' as pageserver config"))?;
                     }
                     _ => bail!(
                         "config file {legacy_config_path} has unrecognized pageserver option '{key}'"
diff --git a/pageserver/src/tenant/config.rs b/pageserver/src/tenant/config.rs
index 4ad6a71f67..7a454b53d2 100644
--- a/pageserver/src/tenant/config.rs
+++ b/pageserver/src/tenant/config.rs
@@ -8,10 +8,12 @@
 //! We cannot use global or default config instead, because wrong settings
 //! may lead to a data loss.
 //!
-use anyhow::Context;
+use anyhow::bail;
 use pageserver_api::models;
 use pageserver_api::shard::{ShardCount, ShardIdentity, ShardNumber, ShardStripeSize};
+use serde::de::IntoDeserializer;
 use serde::{Deserialize, Serialize};
+use serde_json::Value;
 use std::num::NonZeroU64;
 use std::time::Duration;
 use utils::generation::Generation;
@@ -521,105 +523,49 @@ impl Default for TenantConf {
     }
 }
 
-// Helper function to standardize the error messages we produce on bad durations
-//
-// Intended to be used with anyhow's `with_context`, e.g.:
-//
-//   let value = result.with_context(bad_duration("name", &value))?;
-//
-fn bad_duration<'a>(field_name: &'static str, value: &'a str) -> impl 'a + Fn() -> String {
-    move || format!("Cannot parse `{field_name}` duration {value:?}")
-}
-
 impl TryFrom<&'_ models::TenantConfig> for TenantConfOpt {
     type Error = anyhow::Error;
 
     fn try_from(request_data: &'_ models::TenantConfig) -> Result<Self, Self::Error> {
-        let mut tenant_conf = TenantConfOpt::default();
+        // Convert the request_data to a JSON Value
+        let json_value: Value = serde_json::to_value(request_data)?;
 
-        if let Some(gc_period) = &request_data.gc_period {
-            tenant_conf.gc_period = Some(
-                humantime::parse_duration(gc_period)
-                    .with_context(bad_duration("gc_period", gc_period))?,
-            );
-        }
-        tenant_conf.gc_horizon = request_data.gc_horizon;
-        tenant_conf.image_creation_threshold = request_data.image_creation_threshold;
+        // Create a Deserializer from the JSON Value
+        let deserializer = json_value.into_deserializer();
 
-        if let Some(pitr_interval) = &request_data.pitr_interval {
-            tenant_conf.pitr_interval = Some(
-                humantime::parse_duration(pitr_interval)
-                    .with_context(bad_duration("pitr_interval", pitr_interval))?,
-            );
-        }
-
-        if let Some(walreceiver_connect_timeout) = &request_data.walreceiver_connect_timeout {
-            tenant_conf.walreceiver_connect_timeout = Some(
-                humantime::parse_duration(walreceiver_connect_timeout).with_context(
-                    bad_duration("walreceiver_connect_timeout", walreceiver_connect_timeout),
-                )?,
-            );
-        }
-        if let Some(lagging_wal_timeout) = &request_data.lagging_wal_timeout {
-            tenant_conf.lagging_wal_timeout = Some(
-                humantime::parse_duration(lagging_wal_timeout)
-                    .with_context(bad_duration("lagging_wal_timeout", lagging_wal_timeout))?,
-            );
-        }
-        if let Some(max_lsn_wal_lag) = request_data.max_lsn_wal_lag {
-            tenant_conf.max_lsn_wal_lag = Some(max_lsn_wal_lag);
-        }
-        if let Some(trace_read_requests) = request_data.trace_read_requests {
-            tenant_conf.trace_read_requests = Some(trace_read_requests);
-        }
-
-        tenant_conf.checkpoint_distance = request_data.checkpoint_distance;
-        if let Some(checkpoint_timeout) = &request_data.checkpoint_timeout {
-            tenant_conf.checkpoint_timeout = Some(
-                humantime::parse_duration(checkpoint_timeout)
-                    .with_context(bad_duration("checkpoint_timeout", checkpoint_timeout))?,
-            );
-        }
-
-        tenant_conf.compaction_target_size = request_data.compaction_target_size;
-        tenant_conf.compaction_threshold = request_data.compaction_threshold;
-
-        if let Some(compaction_period) = &request_data.compaction_period {
-            tenant_conf.compaction_period = Some(
-                humantime::parse_duration(compaction_period)
-                    .with_context(bad_duration("compaction_period", compaction_period))?,
-            );
-        }
-
-        if let Some(eviction_policy) = &request_data.eviction_policy {
-            tenant_conf.eviction_policy = Some(
-                serde::Deserialize::deserialize(eviction_policy)
-                    .context("parse field `eviction_policy`")?,
-            );
-        }
-
-        tenant_conf.min_resident_size_override = request_data.min_resident_size_override;
-
-        if let Some(evictions_low_residence_duration_metric_threshold) =
-            &request_data.evictions_low_residence_duration_metric_threshold
-        {
-            tenant_conf.evictions_low_residence_duration_metric_threshold = Some(
-                humantime::parse_duration(evictions_low_residence_duration_metric_threshold)
-                    .with_context(bad_duration(
-                        "evictions_low_residence_duration_metric_threshold",
-                        evictions_low_residence_duration_metric_threshold,
-                    ))?,
-            );
-        }
-        tenant_conf.gc_feedback = request_data.gc_feedback;
+        // Use serde_path_to_error to deserialize the JSON Value into TenantConfOpt
+        let tenant_conf: TenantConfOpt = serde_path_to_error::deserialize(deserializer)?;
 
         Ok(tenant_conf)
     }
 }
 
+impl TryFrom<toml_edit::Item> for TenantConfOpt {
+    type Error = anyhow::Error;
+
+    fn try_from(item: toml_edit::Item) -> Result<Self, Self::Error> {
+        match item {
+            toml_edit::Item::Value(value) => {
+                let d = value.into_deserializer();
+                return serde_path_to_error::deserialize(d)
+                    .map_err(|e| anyhow::anyhow!("{}: {}", e.path(), e.inner().message()));
+            }
+            toml_edit::Item::Table(table) => {
+                let deserializer = toml_edit::de::Deserializer::new(table.into());
+                return serde_path_to_error::deserialize(deserializer)
+                    .map_err(|e| anyhow::anyhow!("{}: {}", e.path(), e.inner().message()));
+            }
+            _ => {
+                bail!("expected non-inline table but found {item}")
+            }
+        }
+    }
+}
+
 #[cfg(test)]
 mod tests {
     use super::*;
+    use models::TenantConfig;
 
     #[test]
     fn de_serializing_pageserver_config_omits_empty_values() {
@@ -636,4 +582,38 @@ mod tests {
         assert_eq!(json_form, "{\"gc_horizon\":42}");
         assert_eq!(small_conf, serde_json::from_str(&json_form).unwrap());
     }
+
+    #[test]
+    fn test_try_from_models_tenant_config_err() {
+        let tenant_config = models::TenantConfig {
+            lagging_wal_timeout: Some("5a".to_string()),
+            ..TenantConfig::default()
+        };
+
+        let tenant_conf_opt = TenantConfOpt::try_from(&tenant_config);
+
+        assert!(
+            tenant_conf_opt.is_err(),
+            "Suceeded to convert TenantConfig to TenantConfOpt"
+        );
+
+        let expected_error_str =
+            "lagging_wal_timeout: invalid value: string \"5a\", expected a duration";
+        assert_eq!(tenant_conf_opt.unwrap_err().to_string(), expected_error_str);
+    }
+
+    #[test]
+    fn test_try_from_models_tenant_config_success() {
+        let tenant_config = models::TenantConfig {
+            lagging_wal_timeout: Some("5s".to_string()),
+            ..TenantConfig::default()
+        };
+
+        let tenant_conf_opt = TenantConfOpt::try_from(&tenant_config).unwrap();
+
+        assert_eq!(
+            tenant_conf_opt.lagging_wal_timeout,
+            Some(Duration::from_secs(5))
+        );
+    }
 }