diff --git a/internal/database/database.go b/internal/database/database.go
index 5393f74..acaa6c5 100644
--- a/internal/database/database.go
+++ b/internal/database/database.go
@@ -8,6 +8,7 @@ import (
 	"encoding/json"
 	"errors"
 	"fmt"
+	"math/rand/v2"
 	"net"
 	"net/netip"
 	"os"
@@ -53,6 +54,17 @@ const (
 	sqliteHardHeapLimitBytes = 1610612736
 )
 
+// Bounds on the work GetRandomPrefixesByLength does to pick its sample.
+const (
+	// maxPrefixesToShuffle is the most prefixes of one mask length that are
+	// read in full and shuffled to pick the sample. A mask length with more is
+	// sampled with random lookups, which then seldom land on a prefix twice.
+	maxPrefixesToShuffle = 5000
+	// sampleLookupsPerPrefix is the most random lookups made for each prefix
+	// asked for.
+	sampleLookupsPerPrefix = 4
+)
+
 // Common errors
 var (
 	// ErrInvalidIP is returned when an IP address is malformed
@@ -1696,45 +1708,176 @@ func (d *Database) GetRandomPrefixesByLength(maskLength, ipVersion, limit int) (
 	return d.GetRandomPrefixesByLengthContext(context.Background(), maskLength, ipVersion, limit)
 }
 
-// GetRandomPrefixesByLengthContext returns a random sample of prefixes with context support
+// GetRandomPrefixesByLengthContext returns limit prefixes with the given mask
+// length picked at random, or all of them when there are fewer, each once with
+// its most recently updated live route. However many routes there are, it
+// reads at most maxPrefixesToShuffle+1 prefixes and makes at most
+// sampleLookupsPerPrefix lookups for each prefix asked for.
 func (d *Database) GetRandomPrefixesByLengthContext(
 	ctx context.Context, maskLength, ipVersion, limit int) ([]LiveRoute, error) {
-	// Select unique prefixes with their most recent route information
 	tableName := "live_routes_v4"
 	if ipVersion == ipVersionV6 {
 		tableName = "live_routes_v6"
 	}
 
+	// Reading one prefix more than maxPrefixesToShuffle tells whether these
+	// are all the prefixes with this mask length.
+	prefixes, err := d.firstPrefixesByLength(ctx, tableName, maskLength, maxPrefixesToShuffle+1)
+	if err != nil {
+		return nil, err
+	}
+	rand.Shuffle(len(prefixes), func(i, j int) {
+		prefixes[i], prefixes[j] = prefixes[j], prefixes[i]
+	})
+	if len(prefixes) > maxPrefixesToShuffle {
+		prefixes, err = d.samplePrefixesByLength(ctx, tableName, maskLength, limit, prefixes)
+		if err != nil {
+			return nil, err
+		}
+	}
+	prefixes = prefixes[:min(limit, len(prefixes))]
+
+	return d.newestRouteOfEachPrefix(ctx, tableName, ipVersion, prefixes)
+}
+
+// firstPrefixesByLength returns the first n distinct prefixes, in text order,
+// with the given mask length. It reads only their entries in the mask length
+// and prefix index.
+func (d *Database) firstPrefixesByLength(
+	ctx context.Context, tableName string, maskLength, n int) ([]string, error) {
 	//nolint:gosec // Table name is hardcoded based on IP version
 	query := fmt.Sprintf(`
-		WITH unique_prefixes AS (
-			SELECT prefix, MAX(last_updated) as max_updated
-			FROM %s
-			WHERE mask_length = ?
-			GROUP BY prefix
-			ORDER BY RANDOM()
-			LIMIT ?
-		)
-		SELECT lr.prefix, lr.mask_length, lr.origin_asn, lr.as_path, 
-			lr.peer_ip, lr.last_updated
-		FROM %s lr
-		INNER JOIN unique_prefixes up ON lr.prefix = up.prefix AND lr.last_updated = up.max_updated
-		WHERE lr.mask_length = ?
-	`, tableName, tableName)
+		SELECT DISTINCT prefix FROM %s
+		WHERE mask_length = ?
+		ORDER BY prefix
+		LIMIT ?
+	`, tableName)
 
-	rows, err := d.db.QueryContext(ctx, query, maskLength, limit, maskLength)
+	rows, err := d.db.QueryContext(ctx, query, maskLength, n)
 	if err != nil {
-		return nil, fmt.Errorf("failed to query random prefixes: %w", err)
+		return nil, fmt.Errorf("failed to list prefixes: %w", err)
 	}
-	defer func() {
-		_ = rows.Close()
-	}()
+	defer func() { _ = rows.Close() }()
 
-	var routes []LiveRoute
+	var prefixes []string
 	for rows.Next() {
-		var route LiveRoute
+		var prefix string
+		if err := rows.Scan(&prefix); err != nil {
+			return nil, fmt.Errorf("failed to scan prefix: %w", err)
+		}
+		prefixes = append(prefixes, prefix)
+	}
+	if err := rows.Err(); err != nil {
+		return nil, fmt.Errorf("failed to list prefixes: %w", err)
+	}
+
+	return prefixes, nil
+}
+
+// samplePrefixesByLength picks limit distinct prefixes with the given mask
+// length at random, in at most sampleLookupsPerPrefix lookups for each prefix
+// asked for. ORDER BY RANDOM() would read every route with that mask length.
+// Instead each lookup draws a row id between those of the first and last route
+// with that mask length and takes the prefix of the first such route at or
+// after it. SQLite keeps the row id at the end of every index entry, so the
+// mask length index is ordered by mask length, then row id, and the lookup is
+// one search of it. A prefix with more routes, or with more rows of other mask
+// lengths just before its own, comes up more often: the page needs a varied
+// sample, not an even one. Should the lookups keep landing on prefixes already
+// picked, the rest are taken from shuffled, prefixes of that length in random
+// order.
+func (d *Database) samplePrefixesByLength(
+	ctx context.Context, tableName string, maskLength, limit int, shuffled []string) ([]string, error) {
+	//nolint:gosec // Table name is hardcoded based on IP version
+	rangeQuery := fmt.Sprintf(`
+		SELECT
+			(SELECT MIN(rowid) FROM %[1]s WHERE mask_length = ?),
+			(SELECT MAX(rowid) FROM %[1]s WHERE mask_length = ?)
+	`, tableName)
+
+	var first, last sql.NullInt64
+	if err := d.db.QueryRowContext(ctx, rangeQuery, maskLength, maskLength).Scan(&first, &last); err != nil {
+		return nil, fmt.Errorf("failed to read row id range: %w", err)
+	}
+	if !first.Valid {
+		// Every route with this mask length was withdrawn since they were listed.
+		return nil, nil
+	}
+
+	//nolint:gosec // Table name is hardcoded based on IP version
+	lookupQuery := fmt.Sprintf(`
+		SELECT prefix FROM %s
+		WHERE mask_length = ? AND rowid >= ?
+		ORDER BY rowid
+		LIMIT 1
+	`, tableName)
+
+	stmt, err := d.db.PrepareContext(ctx, lookupQuery)
+	if err != nil {
+		return nil, fmt.Errorf("failed to prepare prefix lookup: %w", err)
+	}
+	defer func() { _ = stmt.Close() }()
+
+	picked := make(map[string]bool, limit)
+	prefixes := make([]string, 0, limit)
+	pick := func(prefix string) {
+		if !picked[prefix] {
+			picked[prefix] = true
+			prefixes = append(prefixes, prefix)
+		}
+	}
+
+	for lookups := 0; lookups < limit*sampleLookupsPerPrefix && len(prefixes) < limit; lookups++ {
+		//nolint:gosec // The sample needs variety, not unpredictability.
+		rowID := first.Int64 + rand.Int64N(last.Int64-first.Int64+1)
+
+		var prefix string
+		err := stmt.QueryRowContext(ctx, maskLength, rowID).Scan(&prefix)
+		if errors.Is(err, sql.ErrNoRows) {
+			// The routes from rowID on were withdrawn since the range was read.
+			continue
+		}
+		if err != nil {
+			return nil, fmt.Errorf("failed to look up prefix: %w", err)
+		}
+		pick(prefix)
+	}
+
+	for _, prefix := range shuffled {
+		if len(prefixes) == limit {
+			break
+		}
+		pick(prefix)
+	}
+
+	return prefixes, nil
+}
+
+// newestRouteOfEachPrefix returns the most recently updated live route of each
+// prefix, one lookup on the prefix index per prefix. A prefix whose routes were
+// all withdrawn since it was picked is left out.
+func (d *Database) newestRouteOfEachPrefix(
+	ctx context.Context, tableName string, ipVersion int, prefixes []string) ([]LiveRoute, error) {
+	//nolint:gosec // Table name is hardcoded based on IP version
+	query := fmt.Sprintf(`
+		SELECT prefix, mask_length, origin_asn, as_path, peer_ip, last_updated
+		FROM %s
+		WHERE prefix = ?
+		ORDER BY last_updated DESC
+		LIMIT 1
+	`, tableName)
+
+	stmt, err := d.db.PrepareContext(ctx, query)
+	if err != nil {
+		return nil, fmt.Errorf("failed to prepare route query: %w", err)
+	}
+	defer func() { _ = stmt.Close() }()
+
+	routes := make([]LiveRoute, 0, len(prefixes))
+	for _, prefix := range prefixes {
+		route := LiveRoute{IPVersion: ipVersion}
 		var pathJSON string
-		err := rows.Scan(
+		err := stmt.QueryRowContext(ctx, prefix).Scan(
 			&route.Prefix,
 			&route.MaskLength,
 			&route.OriginASN,
@@ -1742,17 +1885,16 @@ func (d *Database) GetRandomPrefixesByLengthContext(
 			&route.PeerIP,
 			&route.LastUpdated,
 		)
-		// Set IP version based on which table we queried
-		route.IPVersion = ipVersion
-		if err != nil {
+		if errors.Is(err, sql.ErrNoRows) {
 			continue
 		}
+		if err != nil {
+			return nil, fmt.Errorf("failed to query route of %s: %w", prefix, err)
+		}
 
-		// Decode AS path
 		if err := json.Unmarshal([]byte(pathJSON), &route.ASPath); err != nil {
 			route.ASPath = []int{}
 		}
-
 		routes = append(routes, route)
 	}
 
diff --git a/internal/database/database_test.go b/internal/database/database_test.go
index 82753a9..8ee6463 100644
--- a/internal/database/database_test.go
+++ b/internal/database/database_test.go
@@ -6,6 +6,7 @@ import (
 	"errors"
 	"fmt"
 	"net/netip"
+	"slices"
 	"sync"
 	"testing"
 	"time"
@@ -45,6 +46,19 @@ const (
 	asnSecondBand = 100
 )
 
+// Parameters for the prefix-length sample tests.
+const (
+	// sampleLimit is how many prefixes the tests ask the sample for.
+	sampleLimit = 10
+	// sampledPrefixCount is how many prefixes the sampling test stores, more
+	// than sampleLimit so the sample has to choose among them.
+	sampledPrefixCount = 30
+	// secondV4PeerIP and secondV6PeerIP are the second peer each prefix is
+	// learned from, besides the one mkV4Route and mkV6Route set.
+	secondV4PeerIP = "192.0.2.2"
+	secondV6PeerIP = "2001:db8::2"
+)
+
 // TestGetIPInfoFindsMostSpecificLiveRoute stores nested live prefixes for both
 // families and checks that a lookup returns the most specific one covering the
 // address, ErrNoRoute when none covers it, and the next less specific prefix
@@ -317,3 +331,141 @@ func TestBatchWriteDuringCheckpoint(t *testing.T) {
 	cancel()
 	wg.Wait()
 }
+
+// TestGetRandomPrefixesByLengthListsPrefixOnce stores one prefix of each
+// family learned from two peers in the same second and checks that the
+// prefix-length sample lists each of them once.
+func TestGetRandomPrefixesByLengthListsPrefixOnce(t *testing.T) {
+	cfg := &config.Config{StateDir: t.TempDir()}
+
+	db, err := New(cfg, logger.New())
+	if err != nil {
+		t.Fatalf("failed to create database: %v", err)
+	}
+	defer func() { _ = db.Close() }()
+
+	ts := time.Date(2026, 1, 2, 3, 4, 5, 0, time.UTC)
+	v4First := mkV4Route(t, "198.51.100.0/24", 64500, ts)
+	v4Second := mkV4Route(t, "198.51.100.0/24", 64500, ts)
+	v4Second.PeerIP = secondV4PeerIP
+	v6First := mkV6Route("2001:db8::/32", 64500, ts)
+	v6Second := mkV6Route("2001:db8::/32", 64500, ts)
+	v6Second.PeerIP = secondV6PeerIP
+	if err := db.UpsertLiveRouteBatch([]*LiveRoute{v4First, v4Second, v6First, v6Second}); err != nil {
+		t.Fatalf("UpsertLiveRouteBatch: %v", err)
+	}
+
+	for _, want := range []*LiveRoute{v4First, v6First} {
+		routes, err := db.GetRandomPrefixesByLength(want.MaskLength, want.IPVersion, sampleLimit)
+		if err != nil {
+			t.Fatalf("GetRandomPrefixesByLength(%d, %d): %v", want.MaskLength, want.IPVersion, err)
+		}
+		if len(routes) != 1 || routes[0].Prefix != want.Prefix {
+			t.Errorf("GetRandomPrefixesByLength(%d, %d) = %+v, want %s listed once",
+				want.MaskLength, want.IPVersion, routes, want.Prefix)
+		}
+	}
+}
+
+// TestGetRandomPrefixesByLengthListsNewestRoute stores a prefix learned from
+// two peers at different times, the older route first, and checks that the
+// prefix-length sample lists the newer route.
+func TestGetRandomPrefixesByLengthListsNewestRoute(t *testing.T) {
+	cfg := &config.Config{StateDir: t.TempDir()}
+
+	db, err := New(cfg, logger.New())
+	if err != nil {
+		t.Fatalf("failed to create database: %v", err)
+	}
+	defer func() { _ = db.Close() }()
+
+	older := time.Date(2026, 1, 2, 3, 4, 5, 0, time.UTC)
+	olderRoute := mkV4Route(t, "198.51.100.0/24", 64500, older)
+	newerRoute := mkV4Route(t, "198.51.100.0/24", 64500, older.Add(time.Minute))
+	newerRoute.PeerIP = secondV4PeerIP
+	if err := db.UpsertLiveRouteBatch([]*LiveRoute{olderRoute, newerRoute}); err != nil {
+		t.Fatalf("UpsertLiveRouteBatch: %v", err)
+	}
+
+	routes, err := db.GetRandomPrefixesByLength(newerRoute.MaskLength, ipVersionV4, sampleLimit)
+	if err != nil {
+		t.Fatalf("GetRandomPrefixesByLength: %v", err)
+	}
+	if len(routes) != 1 || routes[0].PeerIP != newerRoute.PeerIP {
+		t.Errorf("GetRandomPrefixesByLength = %+v, want only the newer route, from %s",
+			routes, newerRoute.PeerIP)
+	}
+}
+
+// TestGetRandomPrefixesByLengthSamplesManyPrefixes stores more /24 prefixes
+// than the sample asks for, each followed by a /16 so that routes of another
+// mask length sit between the /24 rows, and each prefix learned from two peers
+// in the same second. It checks both the sample the pages get, picked from the
+// shuffled prefixes, and the random lookups used for a mask length with more
+// than maxPrefixesToShuffle prefixes.
+func TestGetRandomPrefixesByLengthSamplesManyPrefixes(t *testing.T) {
+	cfg := &config.Config{StateDir: t.TempDir()}
+
+	db, err := New(cfg, logger.New())
+	if err != nil {
+		t.Fatalf("failed to create database: %v", err)
+	}
+	defer func() { _ = db.Close() }()
+
+	ts := time.Date(2026, 1, 2, 3, 4, 5, 0, time.UTC)
+	var routes []*LiveRoute
+	var stored []string
+	for i := range sampledPrefixCount {
+		prefix := fmt.Sprintf("10.0.%d.0/24", i)
+		for _, p := range []string{prefix, fmt.Sprintf("172.%d.0.0/16", i)} {
+			first := mkV4Route(t, p, 64500, ts)
+			second := mkV4Route(t, p, 64500, ts)
+			second.PeerIP = secondV4PeerIP
+			routes = append(routes, first, second)
+		}
+		stored = append(stored, prefix)
+	}
+	if err := db.UpsertLiveRouteBatch(routes); err != nil {
+		t.Fatalf("UpsertLiveRouteBatch: %v", err)
+	}
+	slices.Sort(stored)
+
+	maskLength := routes[0].MaskLength
+	sample, err := db.GetRandomPrefixesByLength(maskLength, ipVersionV4, sampleLimit)
+	if err != nil {
+		t.Fatalf("GetRandomPrefixesByLength: %v", err)
+	}
+	var listed []string
+	for _, route := range sample {
+		listed = append(listed, route.Prefix)
+	}
+	checkPrefixSample(t, "GetRandomPrefixesByLength", listed, stored)
+
+	looked, err := db.samplePrefixesByLength(
+		context.Background(), "live_routes_v4", maskLength, sampleLimit, nil)
+	if err != nil {
+		t.Fatalf("samplePrefixesByLength: %v", err)
+	}
+	checkPrefixSample(t, "samplePrefixesByLength", looked, stored)
+}
+
+// checkPrefixSample checks that sample lists sampleLimit prefixes, each once
+// and each one of stored, and that it is not just the first sampleLimit of
+// stored, which is in text order.
+func checkPrefixSample(t *testing.T, name string, sample, stored []string) {
+	t.Helper()
+
+	if len(sample) != sampleLimit {
+		t.Errorf("%s listed %d prefixes, want %d", name, len(sample), sampleLimit)
+	}
+	listed := make(map[string]bool)
+	for _, prefix := range sample {
+		if listed[prefix] || !slices.Contains(stored, prefix) {
+			t.Errorf("%s lists %s twice or it is not one of the /24s", name, prefix)
+		}
+		listed[prefix] = true
+	}
+	if slices.Equal(slices.Sorted(slices.Values(sample)), stored[:sampleLimit]) {
+		t.Errorf("%s lists just the first %d prefixes in text order", name, sampleLimit)
+	}
+}